Species Diversity, Phylogeny and Phylogeography of Centrarchidae

Thomas Near; Jeff Koppelman

Abstract Evolutionary lineages differ with regard to the variety of forms they exhibit. We investigated whether comparisons of morphological diversity can be used to identify differences in ecological diversity in two sister clades of centrarchid fishes. Species in the Lepomis clade (sunfishes) feed on a wider range of prey items than species in the Micropterus clade (black basses).

Chapter 1 Species diversity, phylogeny and phylogeography of Centrarchidae AT ER IA L T. J. Near and J. B. Koppelman 1.1 Introduction CO PY RI GH TE D M Centrarchidae is a clade of freshwater fishes endemic to North America, a part of the world that harbors more species of freshwater fishes than any other nontropical region on Earth (Briggs 1986; Lundberg et al . 2000). Centrarchid fishes have been of interest to biologists for a long period of time because they are commonly the dominant top-level predators in the diverse communities of freshwater fishes in eastern North America, and as such, they are among the world’s most popular freshwater sport fishes (Henshall 1881; Etnier and Starnes 1993; Philipp and Ridgway 2002). Interestingly, it is only in the last 10 years or so that comparative morphological and molecular data have been used in conjunction with objective character-based methods to investigate the phylogenetic relationships of Centrarchidae. The goal of this chapter is to review and assess previous ideas regarding the diversity and relationships of centrarchid species. We hope to provide biologists from all disciplines with a clear picture of the current and best-supported hypotheses of centrarchid phylogeny, and we intend to illustrate how many recent, cutting-edge efforts have agreed remarkably with studies published as far back as the nineteenth century. Although we realize our esoteric interests in centrarchid diversity and phylogeny, as well as our desire to understand the results of modern phylogenetic analyses in the context of the rich past of centrarchid taxonomy and systematics may be confusing to the average fish biologist or ichthyologist, we will attempt to clarify what seems like a morass of trees and classifications for biologists in need of phylogenetic hypotheses. It is our desire that both comparative biologists and conservation agencies exploit the current state of knowledge regarding centrarchid diversity and phylogenetic relationships. In this chapter we provide a discussion of the currently recognized diversity of both extant and fossil species in Centrarchidae, and we attempt to illuminate some unresolved issues in this area that need attention in future research efforts. We present an overview of previous investigations and hypotheses concerning the evolutionary relationships of Centrarchidae, including a discussion of recent efforts using morphological and molecular data in addition to those that pre-date the development of phylogenetic systematics, or cladistics (Hennig 1966). Many of the pre-cladistic ideas of centrarchid relationships discussed in this review were presented as purely taxonomic hypotheses, where the hypothesized relationships were implied from the composition and ranking of taxa. Evolutionary biologists often investigate genetic variation within a geographic context, as intraspecific gene trees often show a strong geographic pattern. Such is the science of phylogeography (Avise 2000). We provide a review and discussion of phylogeography in centrarchids, highlighting some of the problems that have made such analyses in Centrarchidae less straightforward than in species from other groups of North American freshwater fishes. 1.2 Species diversity 1.2.1 Extant species and the status of subspecies Currently, 34 extant species are recognized in Centrarchidae (Table 1.1), with the most recently described species being Ambloplites constellatus and Micropterus cataractae (Cashner and Suttkus 1977; Williams and Burgess 1999). As in 1 2 Centrarchid fishes Table 1.1 Currently recognized centrarchid species and proposed classification. Fossil genera and species are indicated with a dagger. Centrarchidae (44 species: 33 extant, 11 extinct) Centrarchinae Acantharchus pomotis (Baird 1855) Mud sunfish Ambloplites ariommus (Viosca 1936) Shadow bass Ambloplites cavifrons (Cope 1868) Roanoke bass Ambloplites constellatus (Cashner and Suttkus 1977) Ozark bass Ambloplites ruprestris (Rafinesque 1817) Rockbass Archoplites †clarki (Smith and Miller 1985) Clarkia perch Archoplites interruptus (Girard 1854) Sacramento perch Archoplites †molarus (Smith et al. 2000) Ringold sunfish Archoplites †taylori (Miller and Smith 1967) Lake Idaho sunfish †Boreocentrarchus smithi (Schlaikjer 1937) Healy Creek sunfish Centrarchus macropterus (Lacepède 1801) Flier Enneacanthus chaetodon (Baird 1855) Blackbanded sunfish Enneacanthus gloriosus (Holbrook 1855) Bluespotted sunfish Enneacanthus obesus (Girard 1854) Banded sunfish †Plioplarchus septemspinosus (Cope 1889) John Day sunfish †Plioplarchus sexspinosus (Cope 1883) Sentinel Butte sunfish †Plioplarchus whitei (Cope 1883) Laramie sunfish Pomoxis annularis (Rafinesque 1818) White crappie Pomoxis †lanei (Hibbard 1936) Ogallala crappie Pomoxis nigromaculatus (Lesueur 1829) Black crappie Lepominae Lepomis auritus (L 1758) Redbreast sunfish Lepomis cyanellus (Rafinesque 1819) Green sunfish Lepomis gibbosus (L 1758) Pumpkinseed Lepomis gulosus (Cuvier 1829) Warmouth Lepomis humilis (Girard 1858) Orangespotted sunfish Lepomis †kansasensis (Hibbard 1936) Rhino Hill sunfish Lepomis macrochirus (Rafinesque 1819) Bluegill Lepomis marginatus (Holbrook 1855) Dollar sunfish Lepomis megalotis (Rafinesque 1820) Longear sunfish Lepomis microlophus (Günther 1859) Redear sunfish Lepomis miniatus (Jordan 1877) Redspotted sunfish Lepomis peltastes (Cope 1870) Northern longear sunfish Lepomis punctatus (Valenciennes 1831) Spotted sunfish Lepomis †serratus (Smith and Lundberg 1972) Keigh sunfish Lepomis symmetricus (Forbes 1883) Bantam sunfish (continued) Species diversity, phylogeny and phylogeography of Centrarchidae 3 Table 1.1 (continued). Centrarchidae (44 species: 33 extant, 11 extinct) Micropterinae Micropterus cataractae (Williams and Burgess 1999) shoal bass Micropterus coosae (Hubbs and Bailey 1940) Redeye bass Micropterus dolomieu (Lacepède 1802) smallmouth bass Micropterus floridanus (LeSueur 1822) Florida bass Micropterus henshalli (Hubbs and Bailey 1940) Micropterus notius (Bailey and Hubbs 1949), Suwannee bass Micropterus punctulatus (Rafinesque 1819) spotted bass Micropterus †relictus (Cavender and Smith 1975) Chapala bass Micropterus salmoides (Lacepède 1802) largemouth bass Micropterus treculi (Vaillant and Bocourt 1874) Guadalupe bass many groups of animals, there are many more scientific names available than there are recognized species. Not including the names of valid extant species (Table 1.1), there are 118 nominal names that are considered synonyms for species in Centrarchidae. Of these, 11 were either new names for subspecies or were introduced as species names and have been used at some point to designate subspecies (Gilbert 1998). Of the 118 nominal names, 9 are based on hybrid centrarchids; all but 1 of these are the hybrid combinations of Lepomis cyanellus * L. macrochirus and L. cyanellus * L. gibbosus (Hubbs 1920; Hubbs and Hubbs 1932; Gilbert 1998). The contemporary view of species diversity in Centrarchidae was fairly well settled by the turn of the nineteenth and twentieth centuries, as the vast majority of valid centrarchid species were described between 1800 and 1883 (Table 1.1; Figure 1.1). This period was also when most of the synonymous names were introduced (Bailey 1938; Gilbert 1998). Through both the nineteenth and twentieth centuries centrarchid species have been described using very similar types of data from external morphology, including meristics (scale row and fin element counts), morphometrics (body proportions), pigmentation patterns, and coloration (Cope 1868, 1870; Hubbs and Bailey 1940; Cashner and Suttkus 1977; Williams and Burgess 1999). To date, comparative phylogenetic methods, using either morphological or molecular data, have not been used in describing new centrarchid species. No. of valid species described 35 30 25 20 15 Ambloplites rupestris 10 5 1750 1800 1850 1900 1950 2000 Year described Figure 1.1 Plot illustrating the growth of valid extant centrarchid species descriptions from the nineteenth through twentieth centuries. Ambloplites rupestris redrawn from Forbes and Richardson (1920). 4 Centrarchid fishes The status of subspecies in Centrarchidae is much less resolved when compared to the 33 recognized valid extant species (Table 1.1). The use of subspecies in North American fish taxonomy has a relatively inconsistent history, and since the initial critique of subspecies, most modern workers in systematics have been moving away from using this rank (Wilson and Brown 1953; Burbrink et al . 2000). However, there remain 11 names that have been historically designated as centrarchid subspecies. We are able to categorize each of these names into three classes: (i) subspecies that do not exhibit significant variation from the nominal subspecies, (ii) subspecies that are based on hybrid specimens, and (iii) subspecies that merit elevation to species. Three centrarchid subspecies have been invalidated as it was demonstrated that they did not differ appreciably from other populations of the nominal species. Acantharchus pomotis mizelli Fowler and Enneacanthus chaetodon elizabethae were both described as subspecies in the 1940s based on six or seven specimens (Bailey 1941; Fowler 1945). In both cases, subsequent analyses that included many more specimens failed to reveal geographic variation consistent with the recognition of the subspecies proposed for each of these species (Sweeney 1972; Cashner et al . 1989). A similar situation exists for the Neosho Smallmouth Bass, Micropterus dolomieu velox Hubbs and Bailey. This subspecies was described based primarily on slight differences in counts of the second dorsal fin rays, pigmentation patterns, and dentition on the tongue (Hubbs and Bailey 1940). The validity of M. d. velox was subsequently dismissed on the basis of slight morphological differences and clinal gradation into the nominal M. dolomieu (Bailey 1956; Gilbert 1998), a conclusion supported by more recent analyses of nuclear gene encoded allozymes and mitochondrial DNA (mtDNA) sequence data (Stark and Echelle 1998; Kassler et al . 2002). At least one centrarchid subspecies has turned out to be based on hybrid specimens. Micropterus punctulatus wichitae Hubbs and Bailey was described as a subspecies from the Wichita Mountains of southwestern Oklahoma based on differences in scale row counts (Hubbs and Bailey 1940). However, this population was initially described as hybrids of M. punctulatus and M. dolomieu (Hubbs and Ortenburger 1929). Morphological data from M. p. punctulatus, M. p. wichitae, and M. dolomieu and historical records of nonnative M. dolomieu introductions near the type locality of M. p. wichitae support the hypothesis that this subspecies is based on hybrid M. punctulatus * M. dolomieu specimens (Cofer 1995). Genetic analysis of both nuclear and mtDNA in M. punctulatus populations from the Red and Arkansas River Basins did not reveal genetic divergence of the Wichita Mountain populations of M. punctulatus (Coughlin et al . 2003). Lepomis megalotis and L. macrochirus are two centrarchid species that are thought to be polytypic and contain described subspecies (Mayden et al . 1992; Gilbert 1998). Future research documenting morphological and genetic variation in these two complexes has the strong possibility to result in the recognition of additional valid centrarchid species. L. megalotis has four, and possibly seven, valid subspecies, L. m. megalotis (Rafinesque), L. m. aquilensis (Baird and Girard), L. m. breviceps (Baird and Girard), and L. m. occidentalis Meek (Bailey 1938). In addition, L. m. convexifrons (Baird and Girard), L. m. fallax (Baird and Girard), and L. m. popeii (Girard) are three additional forms from Texas that may represent other unrecognized species related to L. megalotis (Gilbert 1998). Unfortunately, there is no published analysis of morphological variation among these subspecies, but a Ph.D. dissertation had detected substantial morphometric variation among four of the described subspecies (Barlow 1980). An analysis of allozyme variation detected appreciable genetic divergence of L. m. breviceps and L. m. aquilensis relative to the other subspecies (Jennings and Philipp 1992). Based on morphometric and body size differences, L. peltastes Cope was elevated as a species from a subspecies of L. megalotis (Bailey et al . 2004). We suspect that several additional centrarchid species will be recognized as a result of analyses of geographic variation and phylogeny of the L. megalotis complex using comparative morphological and molecular data. There is a degree of uncertainty as to how many subspecies of Lepomis macrochirus are recognized. The problem centers on Pomotis speciosus described from Brownsville, Texas by Baird and Girard (1854). This species was subsequently synonymized with L. macrochirus by Hubbs (1935). At a later date, Hubbs and Lagler (1958) treated P. speciosus as a subspecies of L. macrochirus, concluding that the geographic range is throughout Texas and northeastern Mexico. Allozyme analyses did not detect genetic differentiation between L. m. macrochirus and L. m. speciosus (Kulzer and Greenbaum 1986), and subsequent treatments of centrarchid species diversity have not recognized L. m. speciosus (Gilbert 1998). The two valid subspecies of L. macrochirus present an interesting problem of nomenclature confusion, morphological and genetic divergence, an area of presumed secondary contact and introgression, and a biogeographic pattern and a timing of divergence seen in another centrarchid sister species pair. The nominal subspecies L. m. macrochirus Rafinesque is distributed across eastern North America except for the northern Atlantic Coast (Lee et al . 1980), while the other subspecies is endemic to the Florida Peninsula (Felley 1980). Initially, the subspecies found in Florida was designated as Lepomis Species diversity, phylogeny and phylogeography of Centrarchidae 5 macrochirus purpurescens Cope under the premise that this subspecies extended from the Atlantic Coast of the Carolinas to the Florida Peninsula (Hubbs and Allen 1943; Hubbs and Lagler 1958). The type locality for Lepomis purpurescens is in the Yadkin River Drainage in North Carolina (Cope 1870). Subsequent morphological and molecular analyses demonstrate that this is far north of the range of the Florida subspecies (Avise and Smith 1974a; Felley 1980; Avise et al . 1984), and as Gilbert (1998) has pointed out, Cope described a Bluegill from Florida, Lepomis mystacalis (Cope 1877). Therefore, the appropriate name for the Florida Bluegill is L. macrochirus mystacalis. Lepomis m. macrochirus and L. m. mystacalis are morphologically and genetically distinct, but there is a presumed area of introgression through secondary contact along most of southern Georgia and South Carolina (Felley 1980; Avise et al . 1984). Another sister species pair in Centrarchidae, Micropterus salmoides and Micropterus floridanus, exhibit a very similar distribution and area of secondary contact and introgression (Bailey and Hubbs 1949; Philipp et al . 1983). Based on a fossil calibrated molecular phylogeny of Centrarchidae, the divergence time between M. salmoides and M. floridanus is approximately 2.8 million years ago (mya) (Near et al . 2003, 2005b). Lepomis m. macrochirus and L. m. mystacalis exhibit a very similar divergence time. We found mtDNA cytochrome b gene sequences in Genbank for five individuals of L. m. macrochirus and a single L. m. mystacalis (accession numbers: AY115975, AY115976, AY225667, AY828966, AY828967, and AY828968). The average genetic distance between these two subspecies was 4.5%, which translates to a divergence time of roughly 2.3 mya (Near et al . 2003). Future work should aim toward gathering sufficient morphological and molecular data to more precisely determine the geographic distribution of these two forms and assess if L. mystacalis is a valid species. Recently Micropterus henshalli (Hubbs and Bailey) was elevated as a valid species (Baker et al . 2008), but was long recognized as a subspecies of M. punctulatus (Hubbs and Bailey 1940). Micropterus henshalli is endemic to the Mobile Basin and there are slight morphological differences between populations above and below the Fall Line (Gilbert 1973; Baker et al . 2008). However, there are substantial differences in several meristic characters between M. henshalli and M. punctulatus (Gilbert 1973), and there are marked differences in body proportions and surprising life history and dietary differences between these two species (Gilbert 1973). Perhaps the most compelling evidence for the recognition of M. henshalli includes measures of genetic divergence and the results of phylogenetic analyses. Among 19 polymorphic allozyme loci surveyed for all Micropterus species, not a single allele was shared exclusively between M. henshalli and M. punctulatus, and a fixed unique allele was found in M. p. henshalli (Kassler, et al ., 2002). In a phylogenetic analysis of Micropterus species using gap coded continuous morphological characters M. henshalli and M. punctulatus did not form a clade (Harbaugh 1994), and these two species were sister lineages in frequency parsimony of allozyme alleles (Kassler et al . 2002). In addition, molecular phylogenetic analyses of mtDNA sequences from cytb and ND2 resulted in tree topologies where M. henshalli was nested within M. coosae and distantly related to M. punctulatus (Kassler et al . 2002). Given the evidence presented above, the classification of M. henshalli as a subspecies of M. punctulatus was not compelling and the recognition of this species is supported by the substantial comparative data. 1.3 Centrarchid fossils The fossil record of Centrarchidae is fairly rich and extends in geologic time from the Late Eocene to Early Oligocene of approximately 35 mya to the very early Holocene of approximately 10 years ago. Both extant centrarchid species and centrarchid fossils are found only in North America, indicating that origin and diversification of this clade did not involve other continental regions. There are 11 valid and extinct centrarchid species known only from fossil material (Table 1.1; Figures 1.2–1.17), and there are fossils of seven extant species. Despite an excitingly abundant centrarchid fossil record, at least four of the oldest fossil centrarchid species are generally unknown to science. These fossil species are undescribed and have been under study for at least three decades. Unfortunately, they have not been made available to other researchers for study, which has significantly hindered progress in understanding the evolutionary origin of Centrarchidae and its patterns of diversification. The meager information available for these four undescribed fossil species that we present here is from general synopses of the fossil record of North American freshwater fishes (Cavender 1986, 1998). The first of these four we call the High Plains Sunfish, from the northwestern part of Montana near the foothills of the Rocky Mountains. Cavender (1986, 1998) indicates that they are found in Late Eocene to Early Oligocene deposits, but more precise age estimates are unavailable. The High Plains Sunfish has three anal spines and an emarginate caudal fin. The second of these undescribed fossils is the Chadron Sunfish 6 Centrarchid fishes Plioplarchus sexspinosus Figure 1.2 Photos and drawings of fossil Centrarchidae species: †Plioplarchus sexspinosus Sentinel Butte Sunfish, photo redrawn from Eastman (1917). Plioplarchus whitei Figure 1.3 Photos and drawings of fossil Centrarchidae species: †Plioplarchus whitei Laramie Sunfish, redrawn from Cope (1884). Plioplarchus septemspinosus Figure 1.4 Photos and drawings of fossil Centrarchidae species: †Plioplarchus septemspinosus John Day Sunfish, photo redrawn from Eastman (1917). Boreocentrarchus smithi Figure 1.5 Photos and drawings of fossil Centrarchidae species: †Boreocentrarchus smithi Healy Creek Sunfish, redrawn from Schlaikjer (1937). Species diversity, phylogeny and phylogeography of Centrarchidae 7 Pomoxis lanei Figure 1.6 Photos and drawings of fossil Centrarchidae species: Pomoxis †lanei Ogallala Crappie, photo redrawn from Hibbard (1936). Pomoxis sp. Figure 1.7 Photos and drawings of fossil Centrarchidae species: Pomoxis †sp. Wakeeney Crappie, redrawn from Wilson (1968). Archoplites clarkii Figure 1.8 Photos and drawings of fossil Centrarchidae species: Archoplites †clarki Clarkia Perch, photo provided by Smith (1963). Archoplites taylori 2 mm 2 mm 2 mm 2 mm Figure 1.9 Photos and drawings of fossil Centrarchidae species: Archoplites †taylori Lake Idaho Sunfish, redrawn from Miller and Smith (1967). 8 Centrarchid fishes Archoplites molarus 1 cm 1 cm 1 cm 1 cm 1 cm Figure 1.10 Photos and drawings of fossil Centrarchidae species: Archoplites †molarus Ringold Sunfish, redrawn from Smith et al . (2000). Lepomis kansasensis Figure 1.11 Photos and drawings of fossil Centrarchidae species: Lepomis †kansasensis Rhino Hill Sunfish, photo redrawn from Hibbard (1936). Lepomis serratus 2 mm 2 mm 2 mm 1 mm Figure 1.12 Photos and drawings of fossil Centrarchidae species: Lepomis †serratus Keigh Sunfish, redrawn from Smith and Lundberg (1972). Species diversity, phylogeny and phylogeography of Centrarchidae 9 Lepomis sp. A Figure 1.13 Photos and drawings of fossil Centrarchidae species: Lepomis †sp. A Valentine Sunfish, redrawn from Smith (1962). Lepomis sp. B Figure 1.14 Photos and drawings of fossil Centrarchidae species: Lepomis †sp. B Wakeeney Sunfish, redrawn from Wilson (1968). Micropterus relictus Figure 1.15 Photos and drawings of fossil Centrarchidae species: Micropterus †relictus 1975 Chapala Bass, redrawn from Smith et al . (1975). Micropterus sp. B Figure 1.16 Photos and drawings of fossil Centrarchidae species: Micropterus †sp. B Wakeeney Bass, redrawn from Wilson (1968). Micropterus sp. C Figure 1.17 Photos and drawings of fossil Centrarchidae species: Micropterus †sp. C Laverne Bass, redrawn from Smith (1962). 10 Centrarchid fishes from Lower Oligocene limestone deposits in the South Dakota Badlands, dating this fossil to the White River group of approximately 28 to 35 mya (Tedford et al . 1987). The Chadron Sunfish has three anal spines and 27 to 28 vertebrae (Cavender 1986). The third fossil sunfish in this group of undescribed forms is from Lower Miocene deposits in South Dakota, and Cavender (1986) provides an age of approximately 25 mya. These are very similar in morphology to the Chadron Sunfish, but have 29 vertebrae (Cavender 1986). The last of the four undescribed fossils in Cavender (1986) is from Middle Miocene deposits, but no location is given. This fossil species has six or seven anal fin spines and is similar to fossils that were assigned to †Plioplarchus (Cope 1884). There are two extinct genera of Centrarchidae known from the fossil record, †Plioplarchus and †Boreocentrarchus. †Plioplarchus contains three species (Table 1.1), and is the oldest of the described centrarchid fossils (Figures 1.2–1.4). †Plioplarchus sexspinosus and †P. whitei were described from Oligocene age freshwater limestone deposits from the Sentinel Butte of North Dakota (Cope 1883) that date to approximately 30 mya (Feldman 1962) (Figures 1.2 and 1.3). †Plioplarchus sexspinosus and †P. whitei are also found in the Badlands of South Dakota in the White River Group. Specimens that are either †P. sexspinosus or †P. whitei are found at the contact between the Chadron and Brule Formations (Welzenbach 1992), and this is dated to approximately 31 mya (Tedford et al . 1987). †Plioplarchus septemspinosus was described from the John Day River in Oregon (Cope 1889) in the geological deposits that make up the John Day Fauna (Figure 1.4), and is dated between 18 and 31 mya (Tedford et al . 2004). Fossils currently assigned to †P. septemspinosus are also found in the Trout Creek Flora in Oregon and this is dated at 13 mya (Graham 1999). Morphological analyses indicate that †P. septemspinosus from the John Day and Trout Creek locations in Oregon are different from each other and both of these are quite divergent from †P. sexspinosus and †P. whitei (Schlaikjer 1937; Bailey 1938; Smith and Miller 1985). These differences were substantial enough for Bailey (1938) in his unpublished Ph.D. dissertation to describe a new genus for †P. septemspinosus. †Boreocentrarchus smithi was described from Healy Creek, Alaska in deposits that were thought to age from the Oligocene to the Early Miocene (Figure 1.5) (Schlaikjer 1937; Uyeno and Miller 1963), and a more precise estimate of this formation at 24 to 18 mya agrees with these earlier estimates (Merritt 1987). Schlaikjer (1937) argues that †B. smithi is closely related to †P. septemspinosus, but others have questioned whether †B smithi is a centrarchid (Uyeno and Miller 1963). Both †Plioplarchus and †Boreocentrarchus are classified in the Centrarchinae (Table 1.1), because these species possess more than three anal fin spines. Undescribed fossil species in this clade include one from the Horse Creek Fish Quarry in Laramie Co., Wyoming, that dates to approximately 19 mya (Cassiliano 1980), another from the Bear Valley, California (Smith and Miller 1985), and a third from the Humboldt Formation, Nevada, that dates to 9 mya (Smith and Miller 1985; Smith et al . 2002). The remaining centrarchid fossil species are classified in genera that also contain extant species (Table 1.1). Pomoxis is known from the fossil record with one described species, P . †lanei, and one undescribed fossil species. Pomoxis †lanei was found in the Rhino Hill Quarry in Logan Co., Kansas (Hibbard 1936), and age of this fossil formation is correlated with Coffee Ranch mammals that date to 6.6 mya (Wallace 1997; Passey et al . 2002). The holotype of P. †lanei is a complete and crushed skeleton (Figure 1.6). The specimen is a remarkable impression and many morphological features can be scored, counted, or measured (Hibbard 1936). The phylogenetic position of P. †lanei in Pomoxis is unresolved due to conflicting characters. The presence of seven dorsal fin spines and a long dorsal fin base supports the hypothesis that P. †lanei and P. nigromaculatus are sister species (Smith 1962). However, the hypothesis that P. nigromaculatus and P. annularis are sister species is supported by the presence of 17 to 20 anal fin rays in these species versus 12 anal fin rays in P. †lanei (Uyeno and Miller 1963). There is a second fossil species of Pomoxis that is undescribed. These fossils were found in the Wakeeney local fauna that is a part of the Ogallala Formation in Kansas (Wilson 1968). The age of this formation was placed in the lower portion of the Ash Hollow or upper Valentine Formation (Wilson 1968), and this dates to approximately 12 mya (Tedford et al . 2004). These are the oldest Pomoxis fossils and they are fragmentary, consisting of a dentary and premaxillary fragments (Figure 1.7). Archoplites contains three fossil species and only one extant species (Table 1.1). The oldest of the Archoplites fossil species is A. †clarki from the Clarkia Lake Beds in Idaho (Figure 1.8) (Smith and Miller 1985). This fossil formation has been dated at 15.5 mya (Golenberg et al . 1990; Wing 1998). Archoplites †taylori is found in seven different fossil locations in southwestern Idaho and these sites are characterized as lacustrine deposits (Figure 1.9). The oldest of the fossil sites containing A. †taylori is the Poison Creek formation and is dated at 9 mya (Smith and Cossel 2001). The youngest formation containing A. †taylori fossils is Jackass Butte, a part of the Grandview local fauna dated at 2.2 mya (Smith 1975; Lundelius et al . 1987). Archoplites †molarus was recently described from the Ringold Formation Species diversity, phylogeny and phylogeography of Centrarchidae 11 in Washington (Figure 1.10). Fossils of A. †molarus are found at three different locations in the Ringold Formation and the ages of these deposits extend through the Pliocene. Fossils from the White Bluffs local fauna are the oldest at 4.5 mya, the Blufftop Locality and local fauna dates to 3.7 mya, and Tauton Locality dated at 2.9 mya contains the youngest A. †molarus fossils (Smith et al . 2000; Van Tassell et al . 2001). The oldest fossils assigned to the extant species Archoplites interruptus are from the Cache Formation in Lake Co., California and date to the Early Pleistocene, approximately 2.5 mya (Casteel and Rymer 1975). The youngest A. interruptus fossils are from Sacramento Co., California and date to the Pleistocene of approximately 100,000 years ago (Hansen and Begg 1970). There is the possibility of undescribed fossil species of Archoplites. Van Tassell et al . (2001) mention specimens from Grande Ronde Valley in Union Co., Oregon that date to 3.7 mya, and there are other Archoplites fossil specimens dated to the Early or Middle Pleistocene from Moses Lake in Washington (Miller 1965). There are four fossil species of Lepomis, and two of these are closely related to L. gulosus. Lepomis †kansasensis was found in the same fossil formation as P. †lanei, so it is dated at 6.6 mya (Hibbard 1936; Wallace 1997; Passey et al . 2002). The holotype is a nearly complete skeletal impression with a badly crushed head, but morphological features such as dentition can be distinguished (Figure 1.11). The presence of pterygoid teeth in L. †kansasensis led to the original classification of this species in Chaenobryttus that also contained L. gulosus (Hibbard 1936; Bailey 1938). Lepomis †serratus was described from fossils collected at the Keim Formation in the Sand Draw local fauna in Brown Co., Nebraska (Smith and Lundberg 1972). The age of this formation is dated at 3.4 mya (Repenning 1987). The Sand Draw L. †serratus fossils are dentaries, articulars, maxillae, prevomers and preopercles (Figure 1.12). Lepomis †serratus maxillae, prevomers, articulars, and preopercles, premaxillae, and dentaries are also reported from the Seneca local fauna in Hooker Co., Nebraska (Bennett 1979), and this is a younger fossil formation dated between 2.5 and 2.0 mya (Bell et al . 2004). Lepomis †serratus was classified in Chaenobryttus on the basis of morphological similarity of the preopercle with L. gulosus (Smith and Lundberg 1972). The initial classifications proposed for L. †kansasensis and L. †serratus indicate a fairly close phylogenetic affinity with L. gulosus, illustrated by the fact that at one point L. †kansasensis was synonymized with L. gulosus (Branson and Moore 1962). However, Smith and Lundberg (1972) argue that L. †kansasensis is more closely related to other Lepomis species than to L. gulosus, but concur that a definitive conclusion on this issue would result only from a more thorough analysis of the fossil material. There are at least two undescribed Lepomis fossil species. Both of these fossils are quite old and are represented by fragmentary material of the lower jaw. The first of these is referred to as L. †sp. A, and was initially identified as L. cf. microlophus (Smith 1962). The fossil comes from the Lower Valentine Formation in Brown Co., Nebraska (Figure 1.13) (Smith 1962). This fossil location was later identified as the Norden Bridge local fauna (Estes and Tihen 1964), and is dated at 13.5 mya (Tedford et al . 2004). The second undescribed Lepomis fossil species is referred to as L. †sp. B (Figure 1.14), and is found in the same fossil location as the undescribed Pomoxis fossil species discussed earlier (Wilson 1968), so this fossil also dates to approximately 12 mya. There are four fossil Micropterus species, but only one is described. Micropterus †relictus was described from and its jaw element fossils found in Late Pliocene–Early Pleistocene deposits in the Lake Chapala Basin, Mexico (Figure 1.15) (Smith et al . 1975). Micropterus †sp. A consists of fragmentary skull pieces and vertebrae from the Lower Snake Creek fauna in Sioux Co., Nebraska (Matthew 1924), and dates between 16 and 15 mya (Tedford et al . 2004). Micropterus †sp. B was originally identified as M. cf. punctulatus, and the fossil material is a lower pharyngeal jaw and a dentary fragment (Figure 1.16). The fossils were collected in the same formation as Pomoxis †sp. and Lepomis †sp. B and date to 12 mya (Wilson 1968). Micropterus †sp. C. is a dentary from the Laverne Formation in Beaver Co., Oklahoma (Figure 1.17) with an estimated age between 10.5 and 9.5 mya (Smith 1962; Tedford et al . 2004). In addition to A. interruptus discussed earlier, there are at least six extant centrarchid species present in the fossil record. The oldest formations that contain extant species are the Rexroad local fauna in Meade Co., Kansas and the Sand Draw local fauna in Brown Co., Nebraska (Smith 1962; Smith and Lundberg 1972), both dated at 3.4 mya (Bell et al . 2004). These two formations combined contain fossil specimens of Ambloplites rupestris, L. cyanellus, and L. humilis. Both L. cyanellus and L. humilis occur in numerous Pleistocene fossil deposits. Lepomis cyanellus is found in Pleistocene formations ranging in age from 2.3 mya to 10,000 years ago and these sites are spread across Kansas, Michigan, Nebraska, Oklahoma, and Texas (Smith 1954, 1958, 1963; Schultz 1965; Hibbard and Dalquest 1966; Lundberg 1967; Eshelman 1975; Neff 1975; Shoshani and Smith 1996). Pleistocene formations containing L. humilis fossils range in age from 2.5 mya to 250,000 years ago and are restricted to Kansas, Nebraska, and South Dakota (Smith 1963; Ossian 1973; Neff 1975; Bennett 1979; Cross et al . 1986). L. megalotis fossils are found at two Pleistocene fossil formations. The oldest of 12 Centrarchid fishes these two locations is the Rita Blanca Lake Deposit in Hartley Co., Texas and this formation is dated at 2.4 mya (Anderson and Kirkland 1969; Koster 1969; Lindsay et al . 1975; Lundelius et al . 1987; Repenning 1987), whereas the Kanopolis local fauna in Ellsworth Co., Kansas has yielded much younger L. megalotis fossils dated at 300,000 years ago (Neff 1975; Repenning 1987). Micropterus salmoides fossils have been reported from Pleistocene deposits in Kansas, Michigan, and South Dakota that are dated from 300,000 to 14,000 years (Smith 1963; Wilson 1967; Ossian 1973; Neff 1975). Fossil L. gibbosus specimens are known only from a single Pleistocene locality in South Dakota (Ossian 1973). 1.4 Phylogeny 1.4.1 Pre-Cladistic concepts of centrarchid evolutionary relationships The nineteenth century was the time when most of the valid centrarchid species were described (Figure 1.1). Associated with this period of activity was the initial development of hypotheses of centrarchid relationships. In these early studies evolutionary relationships were reflected by the composition of species in particular taxonomic groups that were arranged in nested hierarchical ranks. For example, at the taxonomic rank of family, centrarchids were initially classified with Percidae (Günther 1859), implying a close relationship with pikeperches (Sander), perches (Perca), and darters (e.g., Etheostoma and Percina). The name Ichthelidae was applied to the centrarchids when they were first grouped apart from Percidae as a distinct family (Holbrook 1860). This family name was not used by later authors as Icthelis was regarded as a synonym (Bailey 1938). The first use of the name Centrarchidae came at a time when most of the valid species were described (Cope 1868). Subsequent studies adopted Centrarchidae as the family rank name and presented nested classifications that were meant to imply evolutionary relationships (Jordan 1877; McKay 1881; Bollman 1891). Jordan’s (1877) classification had two subfamilies with one containing Micropterus and all other genera were classified in the second subfamily, Lepominae. Within the Lepominae, the genera Ambloplites, Archoplites, Acantharchus, and Chaenobryttus (Lepomis gulosus) were grouped together. The remaining Lepomis species were classified into five genera that are no longer recognized, and Enneacanthus, Centrarchus, and Pomoxis were placed in the same grouping. The classification presented by McKay (1881) did not include taxonomic ranks above genus. Previous to this classification all Lepomis species were classified into eight genera, Chaenobryttus, Apomotis, Xenotis, Bryttus, Helioperca, Xystroplites, Eupomotis, and Lepomis. McKay (1881) placed all of these species, except for L. gulosus, into Lepomis. The classification presented by Bollman (1891) is important in that it recognized three subfamilies, Centrarchinae, Lepominae, and Micropterinae that are still in use (Table 1.1). Bollman’s (1891) proposed Centrarchinae contained Centrarchus and Pomoxis, whereas the Lepominae contained Archoplites, Ambloplites, Chaenobryttus, Acantharchus, Enneacanthus, Mesogonistius, and Lepomis. Lepomis gulosus was retained in Chaenobryttus as it was considered distantly related to other Lepomis species. The Micropterinae contained two recognized Micropterus species. After the studies of McKay (1881) and Bollman (1891), pharyngeal jaw morphology provided important information for hypotheses of relationships among Lepomis species. Hypertrophied lower pharyngeal arches were presented as evidence to remove L. gibbosus from Lepomis and into the genus Eupomotis (Richardson 1904). A later review of the pharyngeal arches resulted in an amplification of Bollman’s (1891) proposal that all species previously classified in Apomotis, Xenotis, Bryttus, Helioperca, Xystroplites, and Eupomotis were closely related and all species from these genera were placed in Lepomis (Bean and Weed 1911). However, as pointed out by Bailey (1938), some of the discussion in Richardson (1904) and Bean and Weed (1911) was based on hybrid individuals. The first representation of centrarchid relationships presented as a branching dendrogram was in Schlaikjer’s (1937) “suggestions on the phylogeny of the recent Centrarchidae.” This schematic of centrarchid relationships did not result from the current concept of a phylogenetic analysis, but was inferred from body depth, relative mouth size, and numbers of rays and spines on the dorsal and anal fins (Figure 1.18). In this “phylogeny” Centrarchus macropterus was depicted as the ancestral centrarchid species with Pomoxis and Archoplites being represented as early splits from this ancestral lineage. Elongated body shape was an important characteristic that motivated the grouping of Acantharchus, Ambloplites, and Micropterus (including the invalid Huro) (Figure 1.18). In contrast to the classifications of McKay (1881) and Bollman (1891), Schlaikjer (1937) classifies Lepomis species (except L. gulosus) into three genera (Lepomis, Apomotis, and Eupomotis) that were depicted as a group in the branching diagram (Figure 1.18). The Enneacanthus species, including IX(X) Schlaikjer(1937) X 10 10 'Apomotis' symmetricus X 11-12 X III 9 9 Enneacanthus gloriosus 10 III(IV) Mesognistius chaetodon Lepomis auritus 12 XI-XII III 10-11 8-10 III X 10 10-12 Acantharchus pomotis X 9-10 Eupomotis gibbosus 10-11 XI III Chaenobryttus glosus III 10 8-9 10 Ambloplites rupestris 10 VI Huro salmoides 10 VI Pomoxis annularis X 12-15 XII-XIII Archoplites interruptus 15 X VI-VII 18 Micropterus dolomieu VI VII-VIII Pomoxis sparoides VI XI-XIII 15 17-18 12-14 Centrarchus macropterus Figure 1.18 Phylogeny of Centrarchidae presented in Schlaikjer (1937). 15 VII-VIII 13-15 III 10-12 III 13 14 Centrarchid fishes Icthelis Eupomotis Bailey (1938) Helioperca Allotis Bryttus Mesogonistius Lepomis Enneacanthus Pomoxis Lethogrammus Apomotis Centrarchus Acantharchus Chaenobryttus an Micropterus ? ni ni loplitini hi omi rc Lep ra A mb nt h op litin i Huro i in En ne ac mis Ambloplites Arc Ce th Lepo Archoplites Cent rar ch ina e Lep om in ? rini pte ? Micro ae Archoplites interruptus Figure 1.19 Phylogeny of Centrarchidae presented in Bailey (1938). Archoplites interruptus redrawn from Girard (1858). the invalid Mesogonistius, were placed as closely related to Lepomis, with L. gulosus (in Chaenobryttus) outside of this group (Figure 1.18). Bailey (1938) in an unpublished Ph.D. dissertation presented a classification of Centrarchidae and a “hypothetical phylogeny” for the group that was depicted as a branching diagram (Figure 1.19). The characters used by Bailey (1938) were primarily anal fin spines, branchiostegal rays, dentition, body shape, opercle serration, scale morphology, and gill raker morphology. By classifying Centrarchus, Pomoxis, Archoplites, Acantharchus, and Ambloplites in the subfamily Centrarchinae, Bailey (1938) was the first author to propose that species in these genera are closely related (Figure 1.19). The genera Chaenobryttus (L. gulosus), Lepomis, Enneacanthus, Mesogonistius (Enneacanthus chaetodon), Micropterus, and Huro (M. salmoides) were classified together in the subfamily Lepominae (Figure 1.19). Given the uncertainty of Bailey’s (1938) placement of Enneacanthus and Mesogonistius in the phylogenetic tree (Figure 1.19), Lepomis and Chaenobryttus were depicted as the sister lineages and most closely related to Micropterus. Eight subgenera were proposed for ten recognized Lepomis species. Sister species pairs proposed within Lepomis were L. cyanellus–L. symmetricus, L. macrochirus–L. humilis, L. gibbosus–L. microlophus, and L. megalotis–L. marginatus. A detailed “phylogeny” of Lepomis species, as proposed by Bailey (1938), is given in Figure 1.20. A “theoretical phylogeny” was presented in a taxonomic revision of Micropterus that described four new species and subspecies (Figure 1.21; Hubbs and Bailey 1940). This Micropterus “phylogeny” was intuitively derived and based on character variation in scale row and fin counts, and pigmentation patterns (Figure 1.21). In this phylogeny Huro was still used as a monotypic genus to contain M. salmoides. Also, the subspecies of M. punctulatus were not presented as a group that is most closely related to one another (Figure 1.21). This is explained by the fact that Hubbs and Bailey (1940, p. 41) Species diversity, phylogeny and phylogeography of Centrarchidae Bailey (1938) 15 L. gulosus L. cyanellus L. symmetricus L. punctatus L. gibbosus L. microlophus L. humilis L. macrochirus L. auritus Lepomis macrochirus L. megalotis L. marginatus Figure 1.20 Detailed phylogeny of Lepomis presented in Bailey (1938). Subgenera of Lepomis in Figure 1.19 were translated to species names using tables presented in Bailey (1938). Lepomis macrochirus redrawn from Forbes and Richardson (1920). did not rule out a scenario where M. coosae originated through hybridization and introgression between M. dolomieu and M. punctulatus. This explains the “paraphyletic” depiction of M. punctulatus in their branching diagram (Figure 1.21). The phylogeny presented in Bailey (1938) was slightly modified and used to study the evolution of dorsal fin supports in percoid fishes, and particularly in Centrarchidae (Figure 1.22) (Smith and Bailey 1961). In this branching diagram Archoplites is resolved as the sister species of a group containing Pomoxis and Centrarchus (Figure 1.22). The phylogenetic position of Enneacanthus (Mesogonistius was no longer recognized) was still unresolved, but was hypothesized as closely related to Lepomis and Micropterus and not to genera in Centrarchinae (Smith and Bailey 1961). The lateralis system and osteology provided characters for inferences regarding centrarchid phylogeny (Branson and Moore 1962). In this study, relationships were proposed separately for centrarchid genera, species in Lepomis, and species in Micropterus. The “hypothetical dendography” presented as a phylogeny among centrarchid genera is quite different from the hypotheses presented in Bailey (1938) (Figure 1.19) and Smith and Bailey (1961) (Figure 1.22). In Branson and Moore’s (1962) hypothesis, Centrarchinae, as proposed by Bailey (1938), is paraphyletic relative to the Lepominae, and Chaenobryttus is nested outside of a sister group containing Lepomis and Micropterus (Figure 1.23a). Within Lepomis, Branson and Moore (1962) converge on a hypothesis of relationships that is less resolved than Bailey’s (1938) (Figure 1.20), but agree with Bailey (1938) in presenting the L. cyanellus–L. symmetricus and L. macrochirus–L. humilis species pairs (Figure 1.23b). The proposal of relationships among Micropterus species presented by Branson and Moore (1962) agrees with that of Hubbs and Bailey (1940) (Figure 1.21) in depicting M. salmoides as the sister species to all other Micropterus species. Also, Branson and Moore (1962) provide a phylogenetic hypothesis for M. treculi and M. notius (Figure 1.23c), two species that were either not recognized or not described when Hubbs and Bailey (1940) revised Micropterus. The last of the pre-cladistic hypotheses of centrarchid relationships discussed in this review was published after the development of cladistic methods, but is a verbal hypothesis of relationships among Micropterus species based primarily on pigmentation and ecological characteristics (Ramsey 1975). Three lineages in Micropterus were identified and Ramsey’s (1975) hypothesis was converted into a generally unresolved phylogeny. In this tree M. salmoides is grouped by itself, M. coosae and M. dolomieu are sister species, and M. punctulatus, M. treculi, M. notius, and M. cataractae are placed in an unresolved grouping (Figure 1.23d). 16 Centrarchid fishes Hubbs and Bailey (1940) Huro salmoides M.d. dolomieu M.d. velox M. coosae M.p. wichitae M.p. henshalli M.p. punctulatus Micropterus salmoides Figure 1.21 Phylogeny of Micropterus presented in Hubbs and Bailey (1940). Micropterus salmoides redrawn from Forbes and Richardson (1920). 1.4.2 Phylogenetic hypotheses derived from analysis of character data The preceding section reviewed ideas about centrarchid evolutionary relationships that were intuitive, and did not utilize forms of character optimization seen in the current practice of phylogenetic systematics (Swofford et al . 1996). This section reviews more recent hypotheses of centrarchid relationships, and includes those that use a particular optimality criterion to analyze a coded character dataset. As a result of the publication of several studies and datasets over the past 30 years, Centrarchidae has come to provide an exciting system to investigate very relevant issues in systematics such as character congruence among independent molecular datasets (Near et al . 2004), the use of fossil data for calibrating molecular phylogenies (Near et al . 2005b), and the optimal use of phylogenies and divergence time estimates in comparative studies (Bolnick and Near 2005; Collar et al . 2005). The first studies of centrarchid relationships that used a defined optimality criterion to analyze a comparative data matrix were also the first studies to use genetic data in reconstructing centrarchid phylogeny. Allozymes, which are alternative forms of an enzyme produced by different alleles of a given locus that are usually detected by protein electrophoresis, were used to investigate relationships among centrarchid genera and among Lepomis species (Avise and Smith 1974b, 1977; Avise et al . 1977). In these studies allozyme variation was converted to pair-wise genetic distances, and the unweighted pair-group method (UPGMA) was used for cluster analyses that resulted in branching dendrograms. The phylogeny resulting from the UPGMA analysis that included the greatest taxon sampling among these studies is presented in Figure 1.24a (Avise and Smith 1977). These analyses agreed with earlier, pre-cladistic hypotheses by presenting Micropterus and Lepomis as sister lineages (Bailey 1938; Branson and Moore 1962), but Pomoxis grouped with this clade instead of with other Species diversity, phylogeny and phylogeography of Centrarchidae 17 Smith and Bailey (1961) Pomoxis Centrarchus Archoplites CH IN A E Acantharchus EN TR AR Ambloplites Chaenobryttus C LEPOMIN AE ? Lepomis Enneacanthus Micropterus Enneacanthus chaetodon Figure 1.22 Phylogeny of Centrarchidae presented by Smith and Bailey (1961). Enneacanthus chaetodon redrawn from Smith (1907). Centrarchinae (Acantharchus, Archoplites, Centrarchus, and Ambloplites). However, it is important to note that the branch length for this node in the allozyme genetic distance dendrogram was very short (Avise and Smith 1977, Figure 5). The allozyme phylogenies differ from several of the earlier morphological hypotheses in having Enneacanthus closely related to genera comprising Bailey’s (1938) concept of Centrarchinae (Acantharchus, Archoplites, Centrarchus, and Ambloplites), and not Lepomis and Micropterus. Also, relationships within Lepomis were different from the hypotheses presented in Bailey (1938) and Branson and Moore (1962) (Figures 1.20 and 1.23a, b), perhaps most notable is that L. gulosus was nested well within Lepomis, and not in a separate clade that would warrant recognition of Chaenobryttus. A later allozyme study that used a distance Wagner method to construct a centrarchid phylogeny (Parker et al . 1985) resulted in a fairly similar tree (Figure 1.24b). One noticeable difference was the nonmonophyly of Lepomis, a result that may have been an artifact of the genetic distance calculations or the distance clustering method used in this study (Figure 1.24b). Characters from kidney morphology, anal fin spine counts, and olfactory organ morphology were used in the first explicit cladistic analysis of centrarchid phylogeny (Mok 1981). Two separate trees were presented, as Mok (1981) did not combine all the morphological characters for one cladistic analysis. The first phylogeny lacked resolution and was based on five characters from kidney morphology (Figure 1.25a). The presence of an extreme posterior kidney was interpreted as a shared derived character (synapomorphy) for all Centrarchidae except Micropterus. The phylogeny has a basal polytomy with the outgroup taxon (Elassoma), Micropterus, and all other centrarchid genera (Figure 1.25a). Despite the lack of phylogenetic resolution Mok’s (1981) analysis of kidney morphology resulted in a clade containing Centrarchus and Pomoxis that agreed with earlier pre-cladistic hypotheses (Bailey 1938; Smith and Bailey 1961; Branson and Moore 1962). Mok (1981) stressed that the kidney morphology does not support the previous hypotheses that presented Lepomis and Micropterus 18 Centrarchid fishes (a) Branson and Moore (1962) (b) Branson and Moore (1962) L. cyanellus L. symmetricus Archoplites Acantharchus Pomoxis L. humilis L. macrochirus Ambloplites L. punctatus Enneacanthus L. gibbosus L. microlophus Centrarchus Chaenobryttus L. auritus Micropterus L. megalotis Lepomis (c) Branson and Moore (1962) L. marginatus (d) Ramsey (1975) M. salmoides M. salmoides M. dolomieu M. dolomieu M. notius M. coosae M. punctulatus M. coosae M. treculi M. punctulatus M. treculi M. notius M. cataractae Figure 1.23 (a) Phylogeny of centrarchid genera presented by Branson and Moore (1962). (b) Phylogeny of Lepomis presented by Branson and Moore (1962). (c) Phylogeny of Micropterus presented by Branson and Moore (1962). (d) Phylogeny of Micropterus converted from a verbal hypotheses presented by Ramsey (1975). as sister taxa (Bailey 1938; Smith and Bailey 1961; Branson and Moore 1962). The second phylogeny in Mok (1981) was based on two characters, the number of anal spines and folding of the olfactory sac, as presented in Eaton (1956). This tree was also unresolved, but it did argue that more than three anal fin spines was a synapomorphy for Ambloplites, Acantharchus, Archoplites, Centrarchus, and Pomoxis (Figure 1.25b), a result that agreed closely with Bailey’s (1938) concept of Centrarchinae (Figures 1.19 and 1.25b). An undefined set of morphological characters was used for a cladistic analysis of centrarchids, and the resulting tree served as the basis for a comparative study of diet, functional feeding morphology, and behavior (Lauder 1986). The phylogeny had a basal polytomy with Micropterus, Lepomis, and clade containing Pomoxis, Centrarchus, Acantharchus, Archoplites, and Ambloplites (Figure 1.25c). Lepomis was monophyletic and L. gulosus was not closely related to Micropterus. In agreement with Bailey (1938), L. gibbosus and L. microlophus were sister species (Figures 1.20 and 1.25c) The next morphological phylogeny of Centrarchidae was presented in an unpublished Ph.D. dissertation and was based on cladistic analyses of 27 morphological characters (Chang 1988). This phylogeny was pectinate, or completely imbalanced, with Micropterus as the basal sister taxon to all other centrarchids (Figure 1.25d). One interesting aspect of this phylogeny was the placement of Enneacanthus as the sister taxon of the genera that comprise Bailey’s (1938) concept of Centrarchinae, and not closely related to Micropterus or Lepomis. Also, in agreement with several previous studies (Bailey 1938; Smith and Bailey 1961; Mok 1981; Parker et al . 1985), Centrarchus and Pomoxis were sister taxa (Figure 1.25d). Chang’s (1988) study is particularly important because it identified four morphological synapomorphies for Centrarchidae (exclusive of Elassoma), a posterior bifurcation of the swim bladder, the first hemal spine of the same length as the second, a deep groove on the first hemal spine, and contact between the first and second hemal spines. Species diversity, phylogeny and phylogeography of Centrarchidae (a) Avise and Smith (1977) 19 (b) Parker et al. (1985) Acantharchus Acantharchus Archoplites Centrarchus Pomoxis Enneacanthus Centrarchus Ambloplites Pomoxis Micropterus E. obesus E. gloriosus L. humilis L. macrochirus L. gulosus L. macrochirus M. salmoides L. cyanellus M. floridanus L. gibbosus L. punctatus L. auritus L. gulosus L. cyanellus L. microlophus L. megalotis L. marginatus L. microlophus L. punctatus Figure 1.24 (a) Allozyme inferred phylogeny of Centrarchidae presented by Avise and Smith (1977). (b) Allozyme inferred phylogeny of Centrarchidae presented by Parker et al . (1985). In a study examining the evolutionary patterns in functional morphological aspects of feeding in centrarchids, Wainwright and Lauder (1992) used a centrarchid phylogeny that resulted from a cladistic analysis of 53 undefined morphological characters. The tree was similar to that of Chang (1988) in that Micropterus is the basal sister taxon to all other Centrarchidae (Figure 1.26a). Also, in agreement with Bailey’s (1938) concept of Centrarchinae, this phylogeny presented Acantharchus, Ambloplites, Pomoxis, Centrarchus, and Archoplites as a monophyletic group (Figure 1.26a). Archoplites interruptus and C. macropterus were recovered as sister species, a relationship that had not been proposed in any of the previous hypotheses; however, Mok (1981) presented a tree based on olfactory organ folding that had a clade containing Pomoxis, Centrarchus, and Archoplites (Figure 1.25b). Interestingly, in Wainwright and Lauder’s (1992) phylogeny, Enneacanthus was nested within Lepomis and L. gulosus was the phylogenetically basal species in this clade. Some details of the relationships in Lepomis proposed by Wainwright and Lauder (1992) are consistent with previous hypotheses (Bailey 1938; Branson and Moore 1962), and others are unique to this analysis (Figure 1.26a). Mabee (1989, 1993) presented a phylogenetic analysis of Centrarchidae using 61 morphological characters. The trees were used to study the ontogenetic criterion in phylogenetics, asking if an ontogenetic series for a particular character provided a reasonable method to polarize the character in a phylogenetic analysis (Mabee 1989, 1993). From our own reanalysis of the data matrix and other published analyses of this dataset (Mabee 1993; Patterson 1996), it is clear that parsimony analysis using outgroup rooting results in hundreds (if not thousands) of most parsimonious trees. However, a single tree from the set of most parsimonious trees was selected for purposes of Mabee’s (1989, 1993) analyses of ontogenetic character evolution (Figure 1.26b). Despite the seemingly arbitrary nature of the selection of this tree, the strict consensus of the most parsimonious trees is quite well resolved (see Patterson 1996, Figure 1a), and is completely resolute with regard to the details of the phylogenetic relationships discussed in this review. 20 Centrarchid fishes (a) Mok (1981) (kidney morphology) (b) Mok (1981) (anal spines, olfactory organ) outgroup outgroup Micropterus Micropterus Archoplites Enneacanthus Acantharchus Lepomis Ambloplites Acantharchus Enneacanthus Ambloplites Lepomis Archoplites Centrarchus Centrarchus Pomoxis Pomoxis (c) Lauder (1986) (d) Chang (1988) Micropterus Pomoxis Micropterus Lepomis Centrarchus Acantharchus Enneacanthus Archoplites Acantharchus Ambloplites L. gulosus Ambloplites L. cyanellus Archoplites L. macrochirus L. gibbosus L. microlophus Centrarchus Pomoxis Figure 1.25 (a) Phylogeny of Centrarchidae based on a cladistic analysis of kidney morphology presented by Mok (1981). (b) Phylogeny of Centrarchidae based on a cladistic analysis of anal spine counts and scale morphology presented by Mok (1981). (c) Phylogeny of Centrarchidae based on a cladistic analysis of morphological characters presented by Lauder (1986). (d) Phylogeny of Centrarchidae based on a cladistic analysis of 27 morphological characters presented by Chang (1988). The phylogeny presented by Mabee (1989, 1993) is interesting in many respects (Figure 1.26b). In agreement with two of the other morphological cladistic analyses (Chang 1988; Wainwright and Lauder 1992), Micropterus is the sister lineage of all other Centrarchidae. The relationships within Lepomis were very similar to that presented by Wainwright and Lauder (1992)—L. gulosus was the sister species to all others in the clade, and Enneacanthus was nested in Lepomis. Within Lepomis, Mabee’s (1989, 1993) phylogeny has two sister species pairs, L. megalotis–L. marginatus and L. microlophus–L. gibbosus seen in other phylogenies (Bailey 1938; Avise and Smith 1977; Lauder 1986; Wainwright and Lauder 1992); however, the sister species pairs L. macrochirus–L. humilis and L. cyanellus–L. symmetricus proposed by Bailey (1938) and Branson and Moore (1962) were not supported by these analyses (Figure 1.26b). In agreement with many of the earlier, pre-cladistic, morphological hypotheses (Bailey 1938; Branson and Moore 1962), a monophyletic Centrarchinae, exclusive of Enneacanthus, was present in the selected single tree from the pool of most parsimonious trees (Figure 1.26b). However, Acantharchus falls out of this clade in the strict consensus tree (Patterson 1996, Figure 1a). Over the past 5 years DNA data has increasingly been used in phylogenetic analyses of Centrarchidae. Three studies have focused on relationships of Micropterus species (Johnson et al . 2001; Kassler et al . 2002; Near et al . 2003) and have produced fairly congruent results; however, there are some unresolved issues with regard to species recognition in the clade that are illuminated by these molecular studies. Johnson et al . (2001) analyzed the phylogeny of Micropterus species using a maximum parsimony analysis of restriction enzyme digests of whole mtDNA genomes. The monophyly Species diversity, phylogeny and phylogeography of Centrarchidae (a) Wainwright and Lauder (1992) Micropterus Acantharchus Ambloplites Pomoxis Centrarchus Archoplites L. gulosus E. gloriosus E. chaetodon E. obsesus L. cyanellus L. symmetricus L. humilis L. auritus L. megalotis L. marginatus L. macrochirus L. punctatus L. microlophus L. gibbosus 21 (b) Mabee (1993) M. salmoides M. dolomieu M. notius M. punctulatus M. treculi M. coosae Acantharchus P. annularis P. nigromaculatus Centrarchus Archoplites A. rupestris A. cavifrons A. ariommus A. constellatus L. gulosus L. cyanellus L. macrochirus L. symmetricus E. chaetodon E. obsesus E. gloriosus L. humilis L. auritus L. marginatus L. megalotis L. punctatus L. gibbosus L. microlophus Figure 1.26 (a) Phylogeny of Centrarchidae based on a cladistic analysis of morphological characters presented by Wainwright and Lauder (1992). (b) Phylogeny of Centrarchidae based on a cladistic analysis of 61 morphological characters presented by Mabee (1989, 1993). of Micropterus was not tested as only a single outgroup species was used, but the phylogeny depicts M. salmoides as the sister species to all other Micropterus (Figure 1.27a). Near et al . (2003) presented a maximum likelihood analysis of DNA sequences from two mtDNA genes, cytb and ND2 that were collected from 50 individuals sampled from 8 Micropterus species. This maximum likelihood phylogeny was similar to the tree presented by Johnson et al . (2001), but differs primarily where the root was placed. This difference was most likely a consequence of the use of a single outgroup taxon. Also, Johnson et al . (2001) did not provide support values for nodes in the phylogeny, and Near et al . (2003) presented a phylogeny that had most of the interspecific nodes supported with high bootstrap pseudoreplicate scores (Figure 1.27b). In Near et al .’s (2003) tree M. dolomieu and M. punctulatus were sister species, and this clade was sister to the remaining Micropterus species (Figure 1.27b). Differing from Johnson et al . (2001), Near et al . (2003) found M. treculi as the sister species of a clade containing M. salmoides and M. floridanus. There are two aspects of the Micropterus phylogeny presented by Near et al . (2003) that support the recognition of M. floridanus as a species distinct from M. salmoides: (i) the two species exhibit reciprocally monophyletic mtDNA haplotypes, and (ii) the intraspecific branch lengths are shorter than those subtending the interspecific node (Figure 1.27b). Kassler et al . (2002) utilized the sampling of cytb and ND2 mtDNA sequences from Near et al . (2003), but added more M. treculi specimens and included M. henshalli in the phylogenetic analyses. Also, Kassler et al . (2002) presented phylogenies that are derived from the analysis of 19 polymorphic allozyme loci. The mtDNA maximum likelihood phylogeny yielded two very surprising results. First, two distinct M. treculi mtDNA haplotypes were discovered. One of 22 Centrarchid fishes (a) Johnson et al. (2001) (b) Near et al. (2003) M. punctulatus Lepomis macrochirus 100 99 M. salmoides M. dolomieu 100 M. notius 100 Micropterus coosae Micropterus cataractae 100 M. cataractae 100 M. treculi 84 100 100 77 Micropterus notius Micropterus treculi Micropterus salmoides M. dolomieu 96 100 M. punctulatus Micropterus floridanus 0.005 substitutions/site Figure 1.27 (a) Phylogeny of Micropterus based on a cladistic analysis of restriction digests of whole mtDNA genomes presented by Johnson et al . (2001). (b) Phylogeny of Micropterus based on a maximum likelihood analysis of mtDNA gene sequences presented in Near et al . (2003). Outgroup species are not shown. A scale bar for the expected number of substitutions is given in the lower right, and numbers at nodes are percent recovery in a bootstrap analysis. these was resolved as the sister taxon of the clade containing M. floridanus and M. salmoides, and the other was closely related to M. punctulatus. Second, M. henshalli was nested within the haplotypes sampled for M. coosae (Figure 1.28a). These two patterns could be attributed to mtDNA introgression, a process known to occur in fishes (Avise 2001), but the allozyme inferred phylogeny offers some important clues to the unexpected results in the mtDNA phylogeny (Figure 1.28b). In an unpublished study, we have screened 100 M. treculi from three locations within the species’ limited native range and found 49 individuals with the haplotype that is sister to the M. floridanus–M. salmoides clade, and 51 individuals with the haplotype that is closely related to M. punctulatus (Figure 1.28a). There is no geographic pattern within M. treculi as the two haplotypes were found in equal frequency within the three populations sampled. However, regardless of which of the two divergent mtDNA haplotypes are found in a given M. treculi specimen, there is virtually no intraspecific variation among allozyme alleles or DNA sequences from nuclear genes. In the allozyme phylogeny constructed using a frequency parsimony method (Swofford and Berlocher 1987), M. treculi is closely related to M. punctulatus, a result that is expected from the previous classification of M. treculi as a subspecies of M. punctulatus (Hubbs and Bailey 1942). The presence of a divergent mtDNA haplotype that is closely related to the M. floridanus–M. salmoides clade that has no counterpart in the nuclear gene phylogeny (Figure 1.28b) cannot be explained by human introductions of M. punctulatus into the native range of M. treculi. As it stands, the mystery of the two divergent mtDNA haplotypes in the background of what appears to be a homogenous nuclear genome of M. treculi will have to be solved in future studies. The case of M. henshalli, or the Alabama Spotted Bass, is equally puzzling as the pattern revealed in M. treculi. The mtDNA maximum likelihood phylogeny resolves M. p. henshalli as distantly related to M. punctulatus and the haplotypes are nested within M. coosae (Figure 1.28a). Micropterus henshalli and M. coosae are sympatric throughout the Mobile Basin (Mettee et al . 1996; Boschung and Mayden 2004) and the similarity of the mtDNA haplotypes would indicate a Species diversity, phylogeny and phylogeography of Centrarchidae (a) Kassler et al. (2002) (mtDNA) 23 (b) Kassler et al. (2002) (allozymes) M. floridanus M. coosae M. salmoides M. treculi M. notius M. cataractae M. dolomieu M. dolomieu M. floridanus M. punctulatus M. cataractae M. notius M. treculi M. henshalli M. salmoides M. henshalli M. coosae M. punctulatus 0.5 changes M. treculi Figure 1.28 (a) Phylogeny of Micropterus based on a maximum likelihood analysis of mtDNA gene sequences presented by Kassler et al . (2002). Outgroup species are not shown. (b) Phylogeny of Micropterus based on a frequency parsimony analysis of allozyme alleles at 19 loci presented by Kassler et al . (2002). recent introgression of mtDNA from M. coosae to M. henshalli. The allozyme phylogeny resolves M. henshalli as the sister taxon of a clade containing M. punctulatus and M. treculi with a very long branch separating M. henshalli from this clade (Figure 1.28b). In our own work we have collected M. coosae and M. henshalli in sympatry in the upper Coosa River system. These individuals have very similar mtDNA haplotypes (1.3% uncorrected genetic distance), but despite the sympatry of these species the M. p. henshalli haplotypes cluster together exclusive of the paraphyletic M. coosae mtDNA haplotypes (Figure 1.28b). Even if mtDNA introgression is obscuring the true phylogeny of M. henshalli, it is apparent that it is quite distinct from M. punctulatus at nuclear encoded loci (Figure 1.28b) and exhibits substantial morphological divergence (Gilbert 1973). Complete coding sequences from the mtDNA cytb gene were used to examine intraspecific and interspecific relationships of Lepomis species (Harris et al . 2005). All species in the clade, except the very recently elevated L. peltastes, were sampled and multiple individuals were included from each sampled species. As reported by Harris et al . (2005), mtDNA haplotypes from five Lepomis species were not reciprocally monophyletic (Figure 1.29). However, for reasons outlined in the following text, we have found it necessary to reanalyze the cytb data from Harris et al . (2005). The phylogeny presented in this review was obtained using a Bayesian analysis similar to that used by Near et al . (2005b), and we present the phylogeny as a phylogram (Figure 1.29). Harris et al . (2005) state that introgression and the presence of cryptic species best explain the pattern of extensive nonmonophyly observed in Lepomis species. Despite a reasonable probability for this scenario, hybridization cannot be detected without genetic data from nuclear genes or morphological analyses (Neff and Smith 1979; Shaw 2002), and identification of cryptic species would minimally require some degree of assessment of morphological divergence, but such data were not presented (Harris et al . 2005). One possible explanation for the nonmonophyly of Lepomis species not 24 Centrarchid fishes Harris et al. (2005) * * L. auritus group A * * * L. punctatus L. miniatus * L. microlophus * L. miniatus * L. gulosus * Illinois Oklahoma * * L. symmetricus L. cyanellus * L. marginatus group A * * * L. megalotis group A * L. marginatus group B * L. megalotis group C * Maryland L. auritus group B North Carolina * Maryland L. gibbosus West Virginia Minnesota * * * * L. m. macrochirus * 0.05 changes L. auritus group C L. m. mystacalis L. humilis * Figure 1.29 Phylogeny of Lepomis based on a reanalysis of mtDNA gene sequence data presented by Harris et al . (2005). The phylogram resulted from a Bayesian mixed model analysis. Outgroup species are not shown. A scale bar for the expected number of substitutions is given in the lower left, and asterisks at nodes indicate support with significant (0.95) Bayesian posterior probabilities. explored by Harris et al . (2005) is misidentification of specimens. For example, the haplotype of L. symmetricus sampled from McCurtain Co., Oklahoma is very similar (low genetic divergence) to the haplotypes sampled from L. cyanellus (Figure 1.29). Given that L. cyanellus is sympatric with L. symmetricus in this region of Oklahoma (Miller and Robison 2004), specimens of L. cyanellus from the same location as this divergent L. symmetricus haplotype were not sampled, and Harris et al . (2005) do not state that they verified the identification of these specimens together, which means that specimen misidentification cannot be ruled out. The same circumstance can possibly be applied to the phylogenetic resolution of haplotypes from L. auritus group B that nests in the same clade as the sampled L. gibbosus haplotypes (Figure 1.29). The striking similarity of the haplotypes in L. auritus group B and L. gibbosus, in addition to the fact that the two species are sympatric where the L. auritus group B specimens were collected, points to a possible instance of specimen misidentification. Ancestral polymorphism was not considered as a mechanism that could result in the pattern of extensive species nonmonophyly observed in the Lepomis phylogeny (Figure 1.29). Ancestral polymorphism can result in nonmonophyly of a species’ alleles when the ancestral species is polymorphic at the locus, and the random sorting of the alleles during the splitting into multiple daughter species results in a gene tree that is incongruent with the species phylogeny (Neigel and Avise 1986; Pamilo and Nei 1988; Wu 1991; Hudson 1992; Hudson and Coyne 2002). The time to reach coalescence, when the species haplotypes are monophyletic, is proportional to the effective population size. Due to maternal inheritance, the coalescent time for mtDNA haplotypes is one quarter that expected for alleles of an autosomal locus (Moore 1995). One heuristic method to assess if ancestral polymorphism is driving a phylogenetic result is to determine if interspecific branches Species diversity, phylogeny and phylogeography of Centrarchidae 25 (genetic distances) are longer than intraspecific branches in the phylogeny, with the assumption that long interspecific branches indicate that sufficient time has elapsed to expect coalescence and reciprocal monophyly (Moore 1995). The paraphyly of L. miniatus and L. marginatus–L. megalotis are in regions of the Lepomis phylogeny that have fairly short interspecific branch lengths relative to the intraspecific branch lengths, so ancestral polymorphism should not be ruled out as a cause for the observed paraphyly of these species. The first phylogenetic investigation among centrarchid genera using DNA sequences was an analysis of the mitochondrial cytb gene by Roe et al . (2002). The importance of this study was limited by the sampling of only one half of all centrarchid species, and by sparse phylogenetic resolution. Two recent studies have examined relationships of all extant centrarchid species, except the recently elevated L. peltastes and M. henshalli, using DNA sequences from multiple genes. Near et al . (2004) presented phylogenetic trees resulting from maximum parsimony and Bayesian analyses of a three gene data set consisting of the mtDNA, ND2, and two nuclear genes (S7 ribosomal protein intron 1 and the protein coding Tmo4C4 ). Two important conclusions were discussed in Near et al . (2004). First, separate analyses of each of the three sampled gene regions resulted in very similar phylogenies that indicated little incongruence between mtDNA and nuclear gene trees. Second, Shimodaira–Hasegawa tree topology tests indicated that 13 of 20 previous hypotheses of centrarchid relationships examined were significantly different from the best tree that resulted from the Bayesian analysis of the mitochondrial and nuclear gene dataset (Table 1.2). This allowed a unique perspective on how these earlier hypotheses compared in the context of a large set of characters that were sampled for most of the species level diversity in Centrarchidae. The phylogenies inferred from mitochondrial and nuclear gene DNA sequences demonstrated the monophyly of all polytypic genera, and in agreement with earlier studies resolved Lepomis and Micropterus as sister lineages (Bailey 1938; Smith and Bailey 1961; Branson and Moore 1962; Avise and Smith 1977), and provided strong support for a clade containing Enneacanthus Centrarchus, Archoplites, Ambloplites, and Pomoxis (Figure 1.30a, b). Other interesting relationships resolved in these analyses included Archoplites and Ambloplites as sister taxa, and the identification of two sister species pairs within Ambloplites. Relationships within Lepomis were highly resolved and most nodes received strong support in maximum parsimony bootstrap analysis or had significant Bayesian posterior probabilities (Figure 1.30a, b). The sister species pairs L. cyanellus–L. symmetricus and L. humilis–L. macrochirus, proposed by Bailey (1938) and Branson and Moore (1962) (Figures 1.20 and 1.23b), were strongly supported in the mtDNA and nuclear gene phylogenies (Figures 1.30a, b). Also, L. megalotis and L. marginatus were resolved as sister species, supporting the results from several earlier studies (Bailey 1938; Avise and Smith 1977; Mabee 1993). Previous investigations of Lepomis phylogeny have hypothesized that L. microlophus and L. gibbosus are sister species. This relationship was not supported in the mtDNA and nuclear gene phylogenies (Figure 1.30a, b). These two species are the only Lepomis species that exhibit specialized diets, feeding primarily on snails. Both L. microlophus and L. gibbosus possess morphological and behavioral specializations that function in crushing snails (Lauder 1983, 1986; Wainwright and Lauder 1992), and many of these characters had been used as evidence of common ancestry for these two species (Bailey 1938; Branson and Moore 1962; Lauder 1986; Wainwright and Lauder 1992; Mabee 1993). These phylogenies indicated that the evolution of these characters involved with molluscivory have a more complex evolutionary history than previously hypothesized. The dataset used in Near et al . (2004) was expanded to include one additional mitochondrial gene (16S ribosomal RNA) and two additional nuclear genes (calmodulin intron 4 and rhodopsin) for a total of 5553 base pairs of aligned DNA sequence data (Near et al . 2005b). The purpose of this study was to use fossil information to calibrate the molecular phylogeny to estimate divergence times in Centrarchidae. Ten centrarchid fossils were used to provide minimal age estimates for nodes in the phylogeny. Using a fossil cross-validation method (Near and Sanderson 2004; Near et al . 2005a), Near et al . (2005b) were able to identify four fossil calibrations that provided inconsistent molecular age estimates, and six consistent centrarchid fossils were used to calibrate the molecular phylogeny. Molecular divergence times of centrarchid species were estimated using penalized likelihood, a method that account for lineage specific molecular evolutionary rate heterogeneity (Sanderson 2002). The centrarchid phylogeny was presented as a chronogram, where the branch lengths are drawn to reflect estimates of absolute evolutionary ages (Figure 1.31). Given the temporal context of centrarchid diversification, Near et al . (2005b) point out that the origin of Centrarchidae at approximately 35 mya in the late Eocene–early Oligocene corresponds to a time of major global climate change to cooler conditions, and a signature in the fossil record of both lineage extinction and origination for many disparate clades across the tree of life. Another important result from the centrarchid chronogram that was exploited by later studies of functional character evolution and patterns of post-zygotic reproductive isolation was the finding that the major centrarchid lineages had 26 Centrarchid fishes Table 1.2 Shimodaira–Hasegawa tests of alternative phylogenetic hypotheses of centrarchid fishes. Significant results are presented with an asterisk. Hypothesis p Three gene Bayesian phylogeny; Figure 1.30b – Schlaikjer (1937); Figure 1.18 <0.001* Bailey (1938); Figure 1.19 <0.001* Smith and Bailey (1961); Figure 1.22 <0.001* Branson and Moore (1962); Figure 1.23a <0.001* Avise et al. (1977); Figure 1.24a 0.452 Mok (1981); Figure 1.25a <0.001* Mok (1981); Figure 1.25b <0.001* Parker et al. (1985); Figure 1.24b 0.002* Lauder (1986); Figure 1.25c 0.912 Chang 1988; Figure 1.25d 0.472 Wainwright and Lauder (1992); Figure 1.26a <0.001* Mabee (1993); Figure 1.26b <0.001* Lepomis Bailey (1938); Figure 1.20 Branson and Moore (1962); Figure 1.23b <0.001* 0.089 Micropterus Hubbs and Bailey (1940); Figure 1.21 0.014* Branson and Moore (1962); Figure 1.23c <0.001* Ramsey (1975); Figure 1.23d <0.001* Johnson et al. (2001); Figure 1.27a 0.900 Near et al. (2003); Figure 1.27b 0.989 Kassler et al. (2002); Figure 1.28a 0.986 different ages (Bolnick and Near 2005; Collar et al . 2005; Bolnick et al . 2006). For instance, the Centrarchinae (exclusive of Acantharchus) was the oldest major centrarchid clade followed by Lepomis, then Micropterus. Interestingly, despite the fact that Lepomis and Micropterus were sister lineages, the chronogram revealed that the ages of the most recent common ancestor (MRCA) in each clade was quite different with the Lepomis MRCA being substantially older than the MRCA of Micropterus (Figure 1.31). The phylogeny inferred from the expanded mitochondrial and nuclear gene data set presented in Near et al . (2005b) is very similar to those estimated from the earlier mitochondrial and nuclear gene DNA study (Near et al . 2004) (Figures 1.30a, b and 1.31). Important differences included the resolution of Acantharchus pomotis as the sister taxon of all other Centrarchidae (Figure 1.31), where maximum parsimony and Bayesian analyses differed on the placement of this species in the phylogeny in Near et al . (2004) (Figure 1.30a, b). 1.5 Phylogeography Phylogeography investigates the relationships between phylogeny and geography for a species or group of related species. It is an approach to understanding intraspecific geographic subdivision, evolutionary pathways to that subdivision, and Species diversity, phylogeny and phylogeography of Centrarchidae (a) Near et al. (2004) (parsimony) 100 53 50 Acantharchus pomotis Enneacanthus chaetodon Enneacanthus gloriosus 100 Enneacanthus obesus 100 Centrarchus macropterus Archoplites interruptus 91 Ambloplites cavifrons 53 Ambloplites constellatus Ambloplites ariommus 100 100 Ambloplites rupestris Pomoxis annularis 100 Pomoxis annularis Pomoxis nigromaculatus 100 Pomoxis nigromaculatus 100 Pomoxis nigromaculatus 100 Micropterus dolomieu Micropterus dolomieu 100 Micropterus punctulatus Micropterus punctulatus 99 Micropterus notius 100 100 Micropterus notius Micropterus cataractae Micropterus coosae 62 Micropterus treculi Micropterus treculi 100 Micropterus salmoides 78 Micropterus floridanus 97 100 Micropterus floridanus Lepomis auritus 77 Lepomis marginatus 100 Lepomis megalotis 99 Lepomis megalotis 100 100 Lepomis gibbosus Lepomis microlophus 93 Lepomis punctatus 100 Lepomis miniatus 100 100 Lepomis miniatus 100 Lepomis humilis 100 Lepomis humilis Lepomis macrochirus 100 100 Lepomis macrochirus Lepomis gulosus 58 100 Lepomis gulosus Lepomis symmetricus changes 100 Lepomis cyanellus 100 Lepomis cyanellus 100 27 (b) Near et al. (2004) (Bayesian)v * * Centrarchus macropterus Enneacanthus chaetodon Enneacanthus gloriosus Enneacanthus obesus Archoplites interruptus Ambloplites ariommus Ambloplites rupestris Ambloplites cavifrons Ambloplites constellatus Pomoxis annularis Pomoxis annularis Pomoxis nigromaculatus Pomoxis nigromaculatus Pomoxis nigromaculatus Acantharchus pomotis Micropterus dolomieu Micropterus dolomieu Micropterus punctulatus Micropterus punctulatus Micropterus coosae Micropterus cataractae Micropterus notius Micropterus notius Micropterus treculi Micropterus treculi Micropterus salmoides Micropterus floridanus Micropterus floridanus Lepomis gulosus Lepomis gulosus Lepomis symmetricus Lepomis cyanellus Lepomis cyanellus Lepomis humilis Lepomis humilis Lepomis macrochirus Lepomis macrochirus Lepomis auritus Lepomis marginatus Lepomis megalotis Lepomis megalotis Lepomis gibbosus Lepomis microlophus Lepomis punctatus substitutions per site Lepomis miniatus Lepomis miniatus * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * 0.01 * * * * Figure 1.30 (a) Phylogeny of nearly all centrarchid species based on a maximum parsimony analysis of mitochondrial and nuclear gene DNA sequences. The phylogram is a strict consensus of four most parsimonious trees. Outgroup species are not shown. A scale bar for the number of optimized changes is given in the lower left, and numbers at nodes are percent recovery in a bootstrap analysis. (b) Phylogeny of nearly all centrarchid species based on a partitioned mixed-model Bayesian analysis of mitochondrial and nuclear gene DNA sequences. Outgroup species are not shown. A scale bar for the expected number of substitutions is given in the lower left, and asterisks at nodes indicate support with significant (0.95) Bayesian posterior probabilities. geographic patterns of speciation. In simple terms, phylogeography involves putting phylogenies on geographic maps (Avise et al . 1987), and the term was derived to simplify the description of patterns that emerge from co-analysis of a species’ genetic diversity and the geographic framework on which that diversity is distributed. Phylogeography also involves understanding the segregation of genetic diversity under varying conditions of behavioral, physiological, and abiotic separation as they have affected gene flow (Templeton 1998). Both historic and current geographic barriers to dispersal and gene flow have shaped distributional patterns of fish species, and in many instances these patterns are evident across phylogenetically divergent lineages inhabiting the same environments and geographic regions (Avise et al . 1987; Mayden 1987; Strange and Burr 1997; Near et al . 2001). Intraspecific phylogeographic assessments are not without confounding factors. In the case of centrarchid species of recreational fishing importance, stocking over the last 100+ years has spread fish from often-distant sources across virtually all of the major watersheds in North America. Any phylogeographic analysis would have to potentially sort out the admixture of native and introduced genotypes to correctly assess the distribution of diversity. In extreme cases, the original ancestral type could be lost, leaving an anomaly in the genetic landscape (Epifanio and Philipp 2000). For example, a recent study of the distribution of alleles at two loci fixed for M. salmoides and M. floridanus concluded that the extent of mixing was so great in Virginia reservoirs that it was uncertain which species was native (Dutton et al . 2006). 28 Centrarchid fishes Near et al. (2005) * * * * C * * * Acantharchus pomotis Centrarchus macropterus Enneacanthus chaetodon Enneacanthus gloriosus Enneacanthus obesus Pomoxis annularis Pomoxis nigromaculatus Archoplites interruptus Ambloplites ariommus Ambloplites rupestris Ambloplites cavifrons Ambloplites constellatus Micropterus dolomieu Micropterus punctulatus Micropterus cataractae Micropterus coosae Micropterus notius Micropterus treculi Micropterus salmoides Micropterus floridanus Lepomis humilis Lepomis macrochirus Lepomis gulosus Lepomis symmetricus Lepomis cyanellus Lepomis auritus Lepomis marginatus Lepomis megalotis Lepomis gibbosus Lepomis microlophus Lepomis punctatus Lepomis miniatus * C * * * * * * * * C C * * * * C * * C * * * * Eocene Oligocene Early 33.7 Miocene Early Late 28.4 23.8 Middle 16.4 Late 11.2 * * Pi Ps 5.2 2.5 Figure 1.31 Phylogeny of nearly all centrarchid species based on a partitioned mixed-model Bayesian analysis of a seven gene dataset of mitochondrial and nuclear gene DNA sequences. The phylogeny is time-calibrated (chronogram) using six centrarchid fossils to provide minimal age estimates for nodes in the tree. Nodes calibrated with fossils are indicated with a circled ‘‘C.’’ The chronogram is calibrated against the geological time scale. Outgroup species are not shown. Asterisks at nodes indicate support with significant (0.95) Bayesian posterior probabilities. 1.5.1 Phylogeography of Micropterus Although studies of polymorphic genetic loci had been conducted on M. salmoides (Whitt et al . 1971), Philipp et al . (1983) represented the first phylogeographic analysis of a Micropterus species. Based on fixed allelic differences at two allozyme loci, the native range of M. salmoides was divided into three areas that corresponded to M. salmoides, M. floridanus, and intergrades between the two species. Coupled with allele frequency data at two additional allozyme loci, latitudinal clines were revealed that indicate the distribution of populations follows thermal clines (Philipp et al . 1983). Additional allozyme studies on a more-local scale have had mixed results. In South Carolina, variation among sites verified that this region of the Atlantic Slope was an area of intergradation between M. salmoides and M. floridanus, and observed clinal variation appeared to correspond to mean annual temperature (Bulak et al . 1995). However, further north in Virginia, there was no geographic pattern with respect to the fixed alleles that differentiate M. salmoides and M. floridanus, and the authors concluded that this pattern was indicative of either stocking of nonnative species, or that M. salmoides is not native to the region sampled (Dutton et al . 2006). In addition to the two fixed allelic differences, there is substantial mtDNA divergence between M. salmoides and M. floridanus (Nedbal and Philipp 1994; Kassler et al . 2002; Near et al . 2003). Allozyme variation was used to investigate the phylogeography of M. dolomieu across its geographic range, but with a biased sampling of Interior Highlands (Ozark and Ouachita uplands) populations (Stark and Echelle 1998). Substantial genetic heterogeneity among sampling sites was detected (i.e. high Fst values). Multivariate analysis of genetic variation between populations identified four clusters of populations: southwestern Ozarks, northern Ozarks and upper Mississippi, and Ohio drainages, and two distinct Ouachita Highland clusters. Phylogenetic analysis using frequency Species diversity, phylogeny and phylogeography of Centrarchidae 29 parsimony indicated that M. dolomieu populations from northern Ozark rivers were more closely related to populations sampled from the Ohio and Upper Mississippi River Basins than to other Ozark populations (Stark and Echelle 1998). Phylogeographic analysis of western populations of M. punctulatus using mtDNA sequences from the control region and allele frequencies from five microsatellite DNA loci found little genetic variation (Coughlin et al . 2003). However, it was determined that populations from the Arkansas River were more similar to Ouachita River populations, relative to Red River populations. Based on the paleogeography of the river drainages (Mayden 1985, 1988), it was expected that the Red and Ouachita River populations would be most similar genetically. Coughlin et al . (2003) hypothesized mtDNA introgession between M. punctulatus and M. dolomieu because they discovered a shared haplotype. Considering the sister species relationship and recent divergence time between M. punctulatus and M. dolomieu (Kassler et al . 2002; Near et al . 2003, 2005b), we argue that retention of ancestral polymorphism better explains this instance of mtDNA haplotype sharing. Analysis of the mtDNA cytb and ND2 has revealed extensive phylogeographic structuring among populations of the Mobile Basin endemic M. coosae. A small sample of individuals from three different sites in the eastern Mobile Basin exhibited appreciable variation at the mtDNA genes with an estimated intraspecific divergence time of approximately 1.0 mya (Near et al . 2003). Considering that the Mobile Basin is characterized by a substantial number of endemic fish species (Lydeard and Mayden 1995; Mettee et al . 1996; Boschung and Mayden 2004), the discovery of genetic differentiation among such a paltry sampling of M. coosae populations is not surprising. A more thorough phylogeographic analysis based on a sampling of M. coosae throughout its limited geographic range has potential to reveal interesting cryptic diversity. 1.5.2 Phylogeography of Lepomis Despite the fact that most Lepomis species have fairly large geographic ranges, there have been few published studies of intraspecific phylogeography. As discussed in Section 1.2.1 on subspecies, these types of studies have the potential to discover patterns of geographic variation, identify cryptic species, and test species boundaries. The first centrarchid phylogeographic study was Avise and Smith (1974a) who examined allozyme allelic variation in southern L. macrochirus populations. This study revealed an area of intergradation between two described subspecies, L. m. macrochirus and L. m. mystacalis, and genetic differentiation of Texas populations. Subsequent studies have found similar patterns resulting from analyses of mtDNA (Avise and Smith 1977; Avise et al . 1984). Phylogeography of four Lepomis species (L. miniatus, L. punctatus, L. microlophus, and L. gulosus) along the southeastern seaboard of the United States was examined with mtDNA haplotype variation (Bermingham and Avise 1986). Intraspecific patterns in two of these species exhibited phylogeographic discontinuities that were concordant with previously defined biogeographic boundaries identified from the distributional limits of other organisms (Wiley and Mayden 1985). The sister species L. miniatus and L. punctatus exhibited a pattern similar to the intraspecific-level analyses of L. gulosus and L. microlophus with a phylogeographic break at the Apalachicola River (Figure 1.32). Morphological differentiation between the sister species L. miniatus and L. punctatus and between eastern and western populations of L. microlophus is concordant with the mtDNA inferred phylogeographic breaks (Bailey 1938; Warren 1992). The phylogeographic discontinuities exhibited in L. microlophus, L. gulosus, and between L. punctatus and L. miniatus were attributed to sea-level fluctuations along the Costal Plain that had the effect of connecting and isolating costal rivers at different times during the Pliocene and Pleistocene (Bermingham and Avise 1986). The effect of water level fluctuation on the extinction and colonization dynamics of Everglades L. punctatus populations was investigated with allozyme and microsatellite markers (McElroy et al . 2003). As predicted, annual environmental fluctuations in the Everglades of Florida, in the form of water level reductions, led to increases in variation on a local level. Sampling design in this case could have resulted in a very different result if recolonization from areas with higher water levels was not considered (McElroy et al . 2003). In Section 1.2.1 on centrarchid species and subspecies, we discussed that L. megalotis contains four to possibly seven recognized subspecies. The distribution of L. megalotis includes most of the Ohio, middle and lower Mississippi river drainages, and several Gulf of Mexico drainages in Alabama, Mississippi, and Texas. The recent elevation of L. peltastes (Table 1.1; Bailey et al . 2004) based on morphological differences has only partially resolved the problem of the status of subspecies and intraspecific relationships within L. megalotis. Substantial allozyme allelic frequency differences were observed in L. megalotis with differences detected between eastern and western populations (Jennings and Philipp 1992). 30 Centrarchid fishes Lepomis punctatus and L. miniatus 0.08 0.06 0.04 0.02 0.00 P Lepomis punctatus Lepomis miniatus Lepomis microlophus 0.08 0.06 0.04 0.02 0.00 P Lepomis microlophus Figure 1.32 Phylogeography of Lepomis punctatus, L. miniatus, and L. microlophus based on mtDNA haplotype variation (Bermingham and Avise 1986). There were no fixed allelic differences among the populations and subspecies examined, including comparisons involving L. megalotis and L. peltastes. 1.5.3 Phylogeography of Centrarchinae A survey of allozyme variation in A. constellatus, A. rupestris, and A. ariommus came to three conclusions (Koppelman et al . 2000). First, A. constellatus exhibited substantial genetic differentiation from A. rupestris and A. ariommus and is restricted to the White River and sporadic localities in north-flowing tributaries of the upper Osage River. Second, the sister species A. rupestris and A. ariommus did not exhibit any fixed allelic differences at three polymorphic loci. Third, human introductions might have obscured the phylogeographic patterns between A. ariommus and A. rupestris, and may have been responsible for the presence of A. constellatus in the Osage basin (Koppelman et al . 2000). Recently 23 polymorphic microsatellite markers have been isolated from A. interruptus for studies to document population structure. Information on genetic variation is being collected as a prerequisite for efforts to reestablish populations in the species’ native range (Schwartz and May 2004). Given the close phylogenetic relationship between A. interruptus and the four Ambloplites species (Figures 1.30 and 1.31), these microsatellite markers may be helpful in examining the lack of coalescence observed for the allozyme markers between A. rupestris and A. ariommus. 1.6 Conclusions and future directions The vast majority of valid centrarchid species were described in the nineteenth century (Figure 1.1). Despite a long and rich history of species descriptions, taxonomic revisions, and studies aiming to resolve phylogenetic relationships of Centrarchidae, there is still much that is unresolved. Centrarchid fishes are among the most economically important group of freshwater fishes in the world, but many species remain unrecognized. In this review, we have tried to illustrate Species diversity, phylogeny and phylogeography of Centrarchidae 31 that many of these species are probably masquerading as subspecies. A resolution to this problem will only come from published studies that examine morphological and genetic variation within polytypic centrarchid species. With regard to the phylogeny of Centrarchidae, we argue that the analyses using both mitochondrial and nuclear gene sequences provide the best estimates of centrarchid relationships (Figure 1.31). This confidence is based on the near-complete taxon sampling that is not seen in most of the other phylogenetic analyses, a sampling of a large number of characters, congruence between the mitochondrial and nuclear gene phylogenies (Near et al . 2004), and the fact that the DNA dataset is able to reject many of the previous centrarchid phylogenetic relationships (Table 1.2). The most important question facing future phylogenetic studies of Centrarchidae involves the apparent phylogenetic incongruence of the morphological and molecular datasets. For example, the resolution of Enneacanthus as nested in Lepomis is a result in the cladistic analyses of morphology that is never resolved in the DNA inferred phylogenies (Figures 1.26a, b, 1.30a, b, and 1.31). Specifically, combined morphological and DNA character analyses may allow the identification of particular morphological character states that are convergent among centrarchid lineages, and do not reflect common ancestry. Also, it will be useful to compile the morphological characters used in the separate cladistic analyses that presumably did not share many character states (Lauder 1986; Chang 1988; Wainwright and Lauder 1992; Mabee 1993). The mitochondrial and nuclear gene DNA sequence phylogeny is not completely resolved with strongly supported nodes (Figure 1.31). It has been demonstrated that phylogenetic resolution and node support in molecular phylogenies can be increased by adding more base pairs of DNA to the dataset (de Queiroz et al . 2002). In order to increase phylogenetic resolution, we recommend the inclusion of additional mitochondrial and single-copy nuclear gene DNA sequences to the phylogenetic dataset. Given the scientific and economic importance of centrarchids, it is surprising that such little phylogeographic information is available for centrarchid species. The few published studies have provided a glimpse into the cryptic patterns of variation perhaps not readily apparent in external morphological characters. 1.7 Acknowledgments TJN thanks P. C. Wainwright for providing important mentorship and collaboration during the initiation of his centrarchid fish studies. JBK is particularly indebted to D. Philipp for past and current guidance in the conservation genetics of centrarchids. We are grateful to S. Cooke, D. Philipp, D. I. Bolnick, and D. A. Etnier for comments on earlier versions of this review. Research funding was provided by the National Science Foundation (DEB-0716155). References Anderson, R. 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Species Diversity, Phylogeny and Phylogeography of Centrarchidae

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