Chapter 1
Species diversity, phylogeny
and phylogeography of Centrarchidae
AT
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T. J. Near and J. B. Koppelman
1.1 Introduction
CO
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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).
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