Syst. Biol. 57(1):116–130, 2008
c Society of Systematic Biologists
Copyright ISSN: 1063-5157 print / 1076-836X online
DOI: 10.1080/10635150801902193
The Relative Importance of Body Size and Paleoclimatic Change as Explanatory Variables
Influencing Lineage Diversification Rate: An Evolutionary Analysis of Bullhead Catfishes
(Siluriformes: Ictaluridae)
M ICHAEL HARDMAN AND LOTTA M. HARDMAN
Laboratory of Molecular Systematics, Finnish Forest Research Institute, Jokiniemenkuja 1, 01301, Vantaa, Finland; E-mail: [email protected] (M.H.)
Abstract.— We applied Bayesian phylogenetics, divergence time estimation, diversification pattern analysis, and parsimony-based methods of ancestral state reconstruction to a combination of nucleotide sequences, maximum body sizes,
fossils, and paleoclimate data to explore the influence of an extrinsic (climate change) and an intrinsic (maximum body size)
factor on diversification rates in a North American clade of catfishes (Ictaluridae). We found diversification rate to have been
significantly variable over time, with significant (or nearly significant) rate increases in the early history of Noturus. Though
the latter coincided closely with a period of dramatic climate change at the Eocene-Oligocene boundary, we did not detect
evidence for a general association between climate change and diversification rate during the entire history of Ictaluridae.
Within Ictaluridae, small body size was found to be a near significant predictor of species richness. Morphological stasis
of several species appears to be a consequence of a homoplastic increase in body size. We estimated the maximum standard length of the ictalurid ancestor to be approximately 50 cm, comparable to Eocene ictalurids (Astephus) and similar to
modern sizes of Ameiurus and their Asian sister-taxon Cranoglanis. During the late Paleocene and early Eocene, the ictalurid
ancestor diversified into the lineages represented by the modern epigean genera. The majority of modern species originated
in the Oligocene and Miocene, most likely according to a peripheral isolates model of speciation. We discuss the difficulties of detecting macroevolutionary patterns within a lineage history and encourage the scrutiny of the terminal Eocene
climatic event as a direct promoter of diversification. [Clade assymmetry; Eocene extinction; historical biogeography; North
American ichthyofauna; relaxed clock; speciation; Cenozoic freshwater fishes.]
Evolutionary biology aims to understand the factors
that influence diversity and its distribution through
space and time. Much of this understanding is sought
through the identification of extrinsic factors in the environment, intrinsic factors of and among organisms,
and the interaction of these factors through time (e.g.,
Futuyma, 1998; Brock, 2000). As might be expected, the
influence and interaction of extrinsic and intrinsic factors varies among lineages and is not easily determined
without a comprehensive evolutionary analysis (Harvey
and Pagel, 1991).
Although pervasive extrinsic factors such as climate change and continental drift affect biotic systems
broadly, component lineages can respond differently
to a common stimulus (Prothero and Berggren, 1992;
Bradshaw and Holzapfel, 2006). Intrinsic factors such
as body size and thermal tolerance have been the focus of explanations for general trends observed in the
spatial and temporal distribution of vertebrate phenotypes (Allen, 1877; Bergmann, 1847; Cope, 1887; Gloger,
1833). Recent studies using phylogenetically corrected
tests describe both general (Knouft and Page, 2003) and
lineage-specific (Finarelli and Flynn, 2006) evolutionary
responses among North American freshwater fishes and
caniform mammals, respectively. Of the intrinsic factors, maximum body size is believed to be the most
important (Peters, 1983; Schmidt-Nielsen, 1984). However, the relative importance of intrinsic and extrinsic
factors as drivers of diversification is poorly explored
other than for some recent studies of insect-plant interactions (Forest et al., 2007) and flowering plants (Moore
and Donoghue, 2007).
The North American Ichthyofauna and Bullhead
Catfishes (Ictaluridae)
The North American freshwater ichthyofauna is a
model system for the study of patterns and processes
of diversification (Patterson, 1981; Wiley and Mayden,
1985; Mayden, 1987, 1988). The fauna contains contemporary representatives of early actinopterygian lineages (e.g., Acipenser, Polyodon, Amia, and Lepisosteus) as
well as descendants of all the freshwater teleost clades
(osteoglossomorphs, elopomorphs, clupeomorphs, ostariophysans, protacanthopterygians, paracanthopterygians and acanthopterygians; Lee et al., 1980; Page and
Burr, 1991). Of the endemic lineages, bullhead catfishes
(Ictaluridae) are the most species rich.
A recent review of catfish nomenclature considered
there to be seven ictalurid genera containing 64 extant
species and a single genus containing 14 species represented by their fossilized remains (Ferraris, 2007).
Egge and Simons (2006) described Noturus maydeni on
the basis of its geographic separation and distinctive
mitochondrial DNA, bringing the total of the most
species-rich genus in the family to 29 binominals and
with at least one species in the Carolinas awaiting
description (Page and Burr, 1991; Hardman, 2004).
According to Ferraris (2007), Ameiurus is represented
by seven extant and eight fossil species from Oligocene
to Pleistocene deposits in western North America, and
Ictalurus contains nine extant and four fossil species.
However, J. G. Lundberg (personal communication)
considers there to be an additional one to four Mexican
species awaiting description, I. ochoterenai to be a
synonym of I. dugesi, and I. meridionalis to be a distinct
116
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HARDMAN AND HARDMAN—EVOLUTIONARY ANALYSIS OF BULLHEAD CATFISHES
species rather than a synonym of I. furcatus. Pylodictis
olivaris is the sole representative of the genus and known
from Miocene fossils. No fossil material is known of the
cave-dwelling Prietella (two species), Satan eurystomus
or Trogloglanis pattersoni. Fossil ictalurids are known
only from North America, though the family has a sister
taxon found today in southern China and Vietnam (Cranoglanididae: Diogo, 2004; Peng et al. 2005; Hardman,
2005; Sullivan et al., 2006).
Other than the claims made by Matsuo et al. (2001),
ictalurid monophyly is undisputed (Taylor, 1969; Lundberg, 1975, 1985, 1992; Mo, 1991; De Pinna, 1998; Diogo,
2004; Hardman, 2004, 2005; Sullivan et al., 2006). Recent
molecular phylogenetic studies concerning or including
representatives of the family (Hardman and Page, 2003;
Hardman, 2004; Wilcox et al., 2004; Near and Hardman,
2006; Sullivan et al., 2006; Egge and Simons, 2006) have
collectively compiled a nearly complete taxon sample
for mitochondrial gene cytochrome b (cytb) and the second subunit of the nuclear recombination activating gene
(rag2). At the time of this study, sequences of both cytb
and rag2 were unavailable for the southwestern species
of Ictalurus (I. australis, I. balsanus, I. dugesi, I. meridionalis,
I. mexicanus, and I. pricei) and the four cave-dwelling taxa.
Lundberg (1975, 1992) reviewed the fossil record of
Ictaluridae. Though lacking the skull roof synapomorphies of the extant genera, fragments of an undetermined
species of Astephus from late Paleocene-Eocene deposits
of Wyoming provide a minimum age for the family of
approximately 58 Ma. The extinct Ameiurus pectinatus,
from Florissant lake deposits (Eocene-Oligocene boundary) in Colorado, provides a minimum age for Ameiurus
of approximately 35 Ma. The oldest fossils of Ictalurus are
Eocene-Oligocene and from the Cypress Hills Formation
in Saskatchewan. The extant Ictalurus punctatus and Pylodictis olivaris are known to have existed at least as far
back as the middle Miocene, as fossils identified as these
species have been found in beds of South Dakota and
Nebraska, respectively. Pleistocene Noturus are known
from South Dakota.
Given the nearly complete taxon sample of ictalurids
for mitochondrial and nuclear sequence data (Hardman
and Page, 2003; Hardman, 2004; Wilcox et al., 2004;
Near and Hardman, 2006; Sullivan et al., 2006; Egge and
Simons, 2006), ample information concerning their biology, distribution, and systematics (Taylor, 1969; Lee,
et al., 1980; Page and Burr, 1991) and representation in
the fossil record (Lundberg, 1975, 1992), the family is an
attractive candidate for an analysis of the possible roles
played by an extrinsic factor (climate change) and an
intrinsic factor (maximum body size) on their diversification using parametric methods.
Evolutionary Analysis
Methodological developments in ancestral state reconstruction (Harvey et al., 1994; Nee et al., 1994;
Cunningham et al., 1998; Oakley and Cunningham, 2002;
Oakley, 2003; Pagel et al., 2004), divergence time estimation (Drummond et al., 2006; Sanderson, 1998, 2002;
117
Thorne et al., 1998; Cutler, 2000; Kishino et al., 2001;
Thorne and Kishino, 2002, 2005; Yang and Yoder, 2003),
and diversification pattern analysis (Chan and Moore,
2002; Harvey et al., 1994; Moore et al., 2004; Moore and
Chan, 2005; Moore and Donoghue, 2007; Nee et al., 1994,
1996; Paradis, 1997, 1998, 2004) offer a toolbox with which
to obtain statistically robust estimates of ancestral values
and their errors. These parametric approaches integrate
the uncertainty associated with estimates of phylogeny,
branch lengths, fossil ages, and the temporal fluctuation
in rates of speciation, extinction, nucleotide substitution,
and morphological change to reconstruct evolutionary
history and test hypotheses in a statistical framework.
By accommodating rate heterogeneity and fossil or paleogeographic calibration points in their maximum likelihood (ML) or Bayesian inferences, recent studies have
been able to test and develop scenarios of diversification for brachyceran flies (Wiegmann et al., 2003), extinct
moas (Baker et al., 2005), Neotropical placental mammals (Delsuc et al., 2004), modern bird orders in the late
Cretaceous (Pereira and Baker 2006; Slack et al., 2006),
and insect-plant interactions (Forest et al., 2007), as well
as to determine the influence of dispersal and phenotypic innovations on diversification rates in flowering
plants (Moore and Donoghue, 2007) and to explore biotic connections shown by catfishes found today in rivers
of southern Mexico and tropical Africa (Lundberg et al.,
2007). To this list, we add Bullhead catfishes as the focus of an examination of the respective roles played by
Cenozoic climate change and maximum body size on
diversification rate.
Briefly, the objectives of this study were to employ
probabilistic methods of phylogenetic analysis, divergence time estimation, and ancestral state reconstruction
to examine the possible relationships between changes
in diversification rate, ancestral maximum body length,
and paleoclimate during the evolutionary history of
modern ictalurids. To meet these objectives, we used mitochondrial and nuclear protein coding sequences, several fossil calibration points, estimates of maximum body
size from the literature, and a Cenozoic paleoclimate reconstruction based on oxygen isotope data from deep-sea
cores (Zachos et al., 2001).
M ATERIALS AND M ETHODS
Taxon Sampling
We assembled cytb and rag2 sequences (Table 1) deposited at the National Center for Biotechnology Information by Hardman and Page (2003), Hardman (2004),
Waldbieser et al. (2003), Wilcox et al. (2004), Peng et al.
(2005), and Sullivan et al. (2006), aligned them with
Clustal X (Thompson et al., 1997), and checked for unexpected stop codons in MacClade (v.4.0; Maddison and
Maddison, 2000) using appropriate translation codes.
The data set includes the monotypic Pylodictis olivaris,
all species of Ameiurus, all extant species of Noturus except N. crypticus, N. gladiator, and N. stanauli, and three
of nine Ictalurus species. Following the results of Diogo
(2004), Hardman (2005), Peng et al. (2005), and Sullivan
118
TABLE 1. Species, GenBank accession numbers, and source of sequence data. a Peng et al. (2002); b Sullivan et al. (2006); c Hardman and
Page (2003); d Waldbieser et al. (2003); e Hardman (2004); f Wilcox et al.
(2004).
Species
Cranoglanis bouderius
Ameiurus brunneus
Ameiurus catus
Ameiurus melas
Ameiurus natalis
Ameiurus nebulosus
Ameiurus platycephalus
Ameiurus serracanthus
Ictalurus furcatus
Ictalurus lupus
Ictalurus punctatus
Noturus albater
Noturus baileyi
Noturus elegans
Noturus eleutherus
Noturus exilis
Noturus fasciatus
Noturus flavater
Noturus flavipinnis
Noturus flavus
Noturus funebris
Noturus furiosus
Noturus gilberti
Noturus gyrinus
Noturus hildebrandi
Noturus insignis
Noturus lachneri
Noturus leptacanthus
Noturus maydeni
Noturus miurus
Noturus munitus
Noturus nocturnus
Noturus phaeus
Noturus placidus
Noturus stigmosus
Noturus taylori
Noturus sp.(broadtail)
Pylodictis olivaris
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SYSTEMATIC BIOLOGY
cytb
rag2
AF416879a
AY184260c
AY184267c
AY184263c
AY184255c
AY184257c
AY184259c
AY184256c
DQ492401b
AY184251c
AY184249c
AY184252c
AY184248c
AY184250c
AY184247c
AY184246c
AY327075e
AY327076e
AY184245c
AY327077e
AY327079e
AY327080e
AY327082e
AY327083e
AY327081e
AY327084e
AY327085e
AY327086e
AY327087e
AY327088e
AY327089e
AY327090e
AY327091e
AY327092e
AY327093e
AY327094e
AY327078e
AY327095e
AY327096e
AY327097e
AY327098e
AY327099e
AY327100e
AY327101e
AY327102e
AY327103e
AF484159d
AY327267e
AY184253c
AY327268e
AY327272e
AY327274e
AY327278e
AY327280e
AY327276e
AY327283e
AY327284e
AY327288e
AY327291e
AY327292e
AY327294e
AY327295e
AY327298e
AY327301e
AY327304e
AY327305e
AY327271e
AY327306e
AY327309e
AY327311e
AY327315e
AY327317e
AY327319e
AY327321e
AY32732e
AY458887f
et al. (2006), we used Cranoglanis bouderius (Cranoglanididae) as a proximal outgroup. The sequence alignment
is available at http://www.systematicbiology.org.
Phylogeny Estimation
The posterior probability distribution of tree topologies was estimated with the Metropolis-coupled Markov
chain Monte Carlo (MC3 ) algorithm implemented in MrBayes (v3.1.2; Huelsenbeck and Ronquist, 2001; Ronquist
and Huelsenbeck, 2003). Following the recommendations of Shapiro et al. (2006), codon models were applied
to four partitions in the data: (1) first and second positions
of cytb, (2) third positions of cytb, (3) first and second positions of rag2, and (4) third positions of rag2. ModelTest
(v. 3.7; Posada and Crandall, 1998) identified the optimal
model for each partition according to differences in the
Akaike information criterion using parameter estimates
and likelihood scores calculated by PAUP* (v.4.0b10;
Swofford, 2001; Table 2). Given the available settings in
MrBayes, a GTR substitution model was specified when
ModelTest selected submodels of three or more substitu-
TABLE 2. Optimal models identified according to differences in
Akaike information criteria (AIC) by ModelTest, their descriptions,
and closest application in MrBayes as settings permit.
Data
partition
cytb 1st and 2nd
cytb 3rd
rag2 1st and 2nd
rag2 3rd
Optimal
model
TVM+I+
GTR+I+
K80+
TrN+
Base
frequencies
Substitution
classes
Unequal
Unequal
Equal
Unequal
4Tv, 1Ti
4Tv, 2Ti
1 (Ti:Tv)
1Tv, 2Ti
MC3
model
GTR+I+
GTR+I+
K80+
GTR+
tion categories. All state frequencies, substitution rates,
distributions of rate heterogeneity, and the proportion of
invariant sites were sampled separately (when included
in the model) for each data partition. All other priors
were specified with default settings. Two independent
runs of 1 × 107 generations were completed, each containing four chains (three heated incrementally with a
temperature of 0.2) initiated from random starting trees
and sampled every 1 × 103 generations. Upon completion of the runs, convergence to a stationary distribution
was examined by referring to the average standard deviation of split frequencies between paired cold chains and
time series plots of the tree scores (negative log likelihoods). The first 3000 samples (3 × 106 generations) were
discarded as burn-in and the maximum clade credibility
tree (MCC) calculated with TreeAnnotator (v1.4.5r516;
Rambaut and Drummond, 2007). The MCC is preferred
to the 50% majority consensus of post–burn-in samples
as it represents the maximum product of posterior
probabilities of any single tree visited during the MC3
run. Branch support for nodes in the MCC was explored
through reference to nonparametric bootstrap proportions obtained according to ML estimates using the GTR
model applied across all sites combined in a single partition in GARLI (v0.95; Zwickl, 2006, at http://www.bio.
utexas.edu/faculty/antisense/garli/Garli.html). Five
hundred pseudoreplicates were completed, each starting from a random tree and terminating after 1 × 105
generations.
Divergence Time Estimation
According to a likelihood-ratio test (LRT; Langley and
Fitch, 1974) of the MCC and log-likelihood scores estimated by PAUP* (according to models specified by ModelTest for each partition in turn), the ictalurid data set
was found to be overdispersed (2 lnL = 59.49–1136.91,
df = 35, P < 0.001) with respect to a molecular clock.
Given significant rate heterogeneity among lineages, the
95% highest posterior density (HPD) of divergence times
was estimated with a relaxed-clock MCMC approach
(Drummond et al., 2002) using the uncorrelated lognormal (UCLN) model (Drummond et al., 2006) implemented in BEAST (v.1.4.5; Drummond and Rambaut,
2006). Unlike other Bayesian divergence time estimators
the UCLN model does not assume autocorrelation of
substitution rates across nodes, though they are permitted. With respect to node age constraints and absolute
rate calibration, we set conditional lognormal priors with
means and standard deviations of 1.0 and offset values
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HARDMAN AND HARDMAN—EVOLUTIONARY ANALYSIS OF BULLHEAD CATFISHES
119
TABLE 3. Description and fossil basis of lognormal prior distributions of node age constraints specified in the BEAST MCMC analysis
(MRCA = most recent common ancestor). All fossil identifications from Lundberg (1975, 1992) and zero offsets based on stratigraphic ages from
Woodburne (2004).
Zero offset
Mean ± SD
Fossil justification
MRCA: Ictaluridae (root node)
MRCA: Ictalurus + Pylodictis + Noturus
58.0
35
1.1 ± 1.1
1.0 ± 1.0
MRCA: Ictalurus
MRCA: Pylodictis + Noturus
MRCA: A. melas + A. nebulosus
19
19
4
1.0 ± 1.0
1.0 ± 1.0
1.0 ± 1.0
†Astephus sp.: Paleocene-Eocene
†Ictalurus rhaeas: Eocene-Oligocene †Ameiurus
pectinatus: Eocene-Oligocene
Ictalurus punctatus: Miocene
Pylodictis olivaris: Miocene
†Ameiurus sawrockensis: Pleistocene
Constrained node
of 4.0, 19.0, 19.0, 35.0, and a root prior offset of 58.0 with
mean and standard deviation of 1.1 (Table 3). Although
other fossils are available, their morphological generality or distribution in time provide no further information concerning temporal constraints as they are either
younger than the four informative fossils or unable to be
placed phylogenetically.
Two independent and identical BEAST analyses were
completed, each of 1 × 107 generations during which
the posterior probability density of divergence times
was estimated with a UCLN relaxed clock modeling
GTR+I+. All parameters were unlinked and applied
separately to both of two partitions: (1) all first- and
second-codon positions combined, and (2) all third
positions. The prior for the branching process was set
according to a pure birth (Yule) model assuming a constant speciation rate per lineage. A starting chronogram
that satisfied the node age priors was generated by
first importing the MCC annotated with mean branch
lengths from the MC3 analysis into PAUP*, deleting the
outgroup (Cranoglanis bouderius), resetting the root in its
place, and enforcing the resulting phylogram and fossil
calibrations described above in R8S (v. 1.71; Sanderson,
2003). The nonparametric rate smoothing (NPRS)
method (powell algorithm, otherwise default settings)
was used to estimate unknown node ages and provide
an ultrametric tree. The resulting chronogram was
checked in TreeEdit (v1.0a10; Rambaut and Charleston,
2002) to ensure node ages and clades were among those
specified in the prior distributions of the BEAST MCMC
analysis. This chronogram, in newick format, replaced
the UPGMA starting tree in the BEAST input file and
the pertinent text was edited appropriately.
Following completion of the runs, stationarity of each
posterior distribution was examined according to the
marginal probabilities of sampled parameters using
Tracer (v1.3; Rambaut and Drummond, 2003). Given stationary parameter estimates and effective sample sizes
(ESS) >1000, samples from both runs were combined using LogCombiner and the MCC calculated in TreeAnnotator. Samples of the distribution taken prior to stationarity were discarded as burn-in. FigTree (v1.0; Rambaut,
2006) was used to visualize the chronogram and 95%
HPD of divergence times.
Patterns and Rates of Lineage Diversification
Following Moore and Donoghue (2007), shifts in lineage diversification rate through time were evaluated us-
ing both temporal and topological approaches. Temporal
methods involve the distribution of node ages through
time and calculation of the relative cladogenesis statistic
(Nee et al., 1996; Moore and Donoghue, 2007) in END-EPI
(Rambaut et al., 1997). The topological method examined
the MCC branching pattern and a sample of 1000 trees
drawn from the stationary distribution of the MC3 analysis for significant changes in diversification rate by calculating shift statistics (1 ) and performing whole-tree
tests of diversification rate variation using SymmeTREE
(v1.1; Chan and Moore, 2005). The null distribution for
each test statistic was generated by Monte Carlo simulation of 1 × 106 trees containing the same number of
taxa as the test tree and branching according to an equalrates Markov (ERM) model. In order to explore issues associated with taxon sampling in the diversification rate
analysis (e.g., Nee et al., 1996), an experiment following
that outlined by Moore and Chan (2005) and Moore and
Donoghue (2007) was completed by assigning the missing extant species to their respective supraspecific taxa
as far as they are known. The missing extant Ictalurus
species were assigned according to the synthetic phylogeny of Lundberg (1992); i.e., I. balsanus and I. meridionalis in a trichotomy along with I. furcatus; and I. australis,
I. dugesi (including I. ochoterenai), I. mexicanus, and I. pricei in an unresolved node subtending these species as
well as the sampled I. punctatus and I. lupus. Similarly,
Noturus crypticus and N. stanauli were assigned to a polychotomous node subtending these two species; and N.
baileyi, N. elegans, N. fasciatus, N. hildebrandi, and N. gladiator as sister to N. stigmosus following Hardman (2004),
Near and Hardman (2006), and Egge and Simons (2006).
Soft polytomies were randomly resolved 1 × 106 times
according to the taxon-size-sensitive ERM model (Chan
and Moore, 2002; Moore and Chan, 2005).
Reconstruction of Ancestral Body Size and Its
Correspondence to Species Richness
Body size has been identified as one of the most
important intrinsic factors governing animal biology
(Schmidt-Nielsen, 1984) and one that has exhibited directional evolutionary trends among families of North
American freshwater fishes (Knouft and Page, 2003).
The extant and reconstructed evolution of maximum
standard length (MSL; body length excluding the caudal fin) was examined with respect to the MCC from
the BEAST MCMC analysis and compared to the
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results of the diversification rate analysis and changes
in Cenozoic climate. We collected MSLs from Page and
Burr (1991), Thomas and Burr (2004), Burr et al. (2005),
and Egge and Simons (2006; see Fig. 2). These continuous data were natural-log–transformed prior to being
analyzed according to MCMC methods in BayesTraits
(http://www.evolution.reading.ac.uk/; Pagel et al.,
2004) and weighted-squared-change parsimony (WSP;
Maddison, 1991) in Mesquite (v. 1.12; Maddison and
Maddison, 2006). Additionally, MacroCAIC (v. 1.0.1;
Agapow and Isaac, 2002) was used to evaluate the relationship between species richness and lnMSL through
the comparison of independent contrasts (Felsenstein,
1985; Harvey and Pagel, 1991; Garland et al., 1992).
BayesTraits was used to examine the evolution of lnMSL across the post–burn-in phylograms from the MC3
analysis. Prior to their input to BayesTraits, the sample of
phylograms was thinned to 4.0 × 103 and rooted according to the outgroup (Cranoglanis bouderius) in Mesquite
so that the ingroup node was dichotomous and the outgroup had a positive branch length. A total of 2 × 107
iterations, sampled every 1 × 103 , were completed and
the number of generations required to reach stationarity of the posterior distribution detected by examining
marginal probabilities plotted as time series in TRACER.
The “ratedev” prior was set heuristically so that the mean
acceptance of the proposed state was at least 25% in the
posterior distribution. This parameter enables the chain
to be effectively mixed when stationary. All other priors were uniformly distributed. Three replicate MCMC
runs were completed to estimate the distribution of likelihood scores of nested hypotheses in which the lnMSL
data evolved according to a random-walk or a directional model of evolution across the samples of MC3
phylograms. Bayes factors (BFs) were used to assess relative support for the alternative (directional) and null
(random-walk) hypotheses, calculated as twice the difference between the harmonic mean of the marginal log
likelihood under the corresponding model (e.g., Suchard
et al., 2001). The preferred evolutionary model was then
used to estimate the mean values of posterior distributions of three scaling parameters: delta (δ; ancient or recent trait evolution), kappa (κ; rate heterogeneity in trait
evolution), and lambda (λ; phylogenetic signal in trait
evolution; Pagel, 1994, 1997, 1999).
Unfortunately, BayesTraits can only reconstruct ancestral states for discretely coded data; e.g., binary or
multistate. In its place, the WSP method was used to
reconstruct ancestral states of lnMSL on the MCC in
Mesquite. WSP minimizes the sum of squared changes
occurring tip-to-node and node-to-node weighted according to their branch length (Maddison, 1991). By incorporating branch lengths, WSP mimics an ML estimate
of the same assuming a Brownian motion evolutionary
process (Finarelli and Flynn, 2006). Following the detection of significant phylogenetic structure (λ ≈ 1.0), the
PDAP module (Midford et al., 2005) was used to estimate standard errors and confidence intervals for the
ancestral lnMSLs following Garland et al. (1999).
In order to evaluate the extent to which lnMSL predicts species richness among ictalurids, least-squares regression through the origin (Garland et al., 1992) of 24
independent contrasts (sister-species comparisons are
uninformative) was completed in MacroCAIC using the
MCC with branch lengths in units of time following the
recommendations of Isaac et al. (2003). Differences in
clade species richness were measured according to the
relative rate difference statistic (RRD = ln[ni /n j ], where
ni is the number of species in the larger clade, and n j
the number in the smaller clade; Gittleman and Purvis,
1998; Isaac et al., 2003). The ancestral reconstruction of lnMSL was made according to a Brownian motion model of
character change, as in WSP, with branch lengths taken
between point estimates of node ages from the BEAST
MCMC analysis. Similar to Gittleman and Purvis (1998),
the extent to which species richness was dependent on a
particular value of lnMSL was tested by regressing RRD
against reconstructed values of lnMSL. Also, to examine
the extent to which the association was constant through
time, RRD was regressed against node age.
Paleoclimatic Change and Its Relationship
to Diversification Rate
To explore the correspondence of possible associations
between changes in climate and natural log per lineage
accumulation rate (lnλ) during the Cenozoic, mean ocean
temperature (MOT) changes were collected from the
paleoclimate reconstruction of Zachos et al. (2001) and
changes in the lnλ from the MCMC chronogram for each
of 58 one-million-year intervals. Given that the analysis
does not include an estimate of the per lineage extinction rate, lnλ is based solely on lineage birth and thus
assumes either positive (speciation) or neutral (no speciation) values. Changes in MOT on the other hand can
be positive, neutral or negative. Observations of the six
possible pairings were scored and exposed to a standard
χ 2 test of the null hypothesis of no association between
the change in MOT and change in lnλ. Additionally, the
correspondence between these two variables based on
the absolute rate of change in MOT (±◦ C per million
years) was examined according to a two-tailed test using Kendall’s τb correlation coefficient.
R ESULTS
Phylogeny
After approximately 3 × 106 generations, the average
standard deviation between split frequencies of the coupled runs stabilized with stochastic fluctuation between
0.0045 and 0.007, suggesting convergence to the stationary distribution. Accordingly, the first 3 × 104 samples
were discarded as burn-in. All parameter estimates of the
post burn-in sample had ESS values >1000. The MCC of
the MC3 analysis was made ultrametric in r8s and specified as starting tree for the MCMC analysis in BEAST.
Given the inclusion of additional prior information, i.e.,
node age distributions, the MCC obtained from the
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HARDMAN AND HARDMAN—EVOLUTIONARY ANALYSIS OF BULLHEAD CATFISHES
post–burn-in sample of the BEAST MCMC analysis was
considered the best estimate of phylogeny. Figure 1 displays the results of the divergence time reconstruction,
and Fig. 2 the cladogram containing node posterior probabilities (PPs) and proportion of 500 ML bootstrap pseudoreplicates (MLBPs) estimated by GARLI.
In the MCC, all genera were recovered monophyletic
with convincing support (PPs and MLBPs of 1.0 and
0.99 to 1.0, respectively). Ameiurus was resolved as the
basal genus and Ictalurus as sister to Noturus and Pylodictis. Though intergeneric nodes all had PPs of 1.0,
only the clade comprising Noturus and Pylodictis was
found in more than 0.5 of MLBPs (0.72). Relationships
among Ameiurus species were resolved as in Hardman
and Page (2003) and relationships among the incompletely sampled Ictalurus were consistent with those of
previous studies based on morphology (Lundberg, 1970,
1992). Ictalurus furcatus was found to be sister to a clade
of the widespread I. punctatus and the southwestern I.
lupus. Pylodictis is monotypic and its recovery as sister
to Noturus is consistent with the morphological studies
of Taylor (1969) and Lundberg (1975, 1982, 1992). Relationships among Noturus species were similar to those
inferred from analyses of similar data sets (Hardman,
2004; Burr et al., 2005; Near and Hardman, 2006; Egge
and Simons, 2006) and a survey of allozyme and chromosomal variation (Grady and LeGrande, 1992).
Divergence Time Estimates
Stationarity of each of the BEAST MCMC posterior
distributions was examined by plotting time series of the
marginal probabilities of estimated parameters. Samples
of the first 2.0 × 106 generations were discarded as burnin and subsequent ESSs of all parameters were at least
1.3 × 103 . The MCC of combined samples with the stationary distribution is shown in Fig. 1. The mean ± standard deviation width of the 95% HPDs was 11.8 ± 4.7 Ma.
Error widths were positively correlated with node age
(B = 2.22, SE = 0.237, t = 9.38, P < 0.001); thus, more
ancient nodes were less precisely estimated. Overall, the
chronology describes a scenario in which the modern
ictalurid lineages originated early in the Eocene and
that the majority of extant species originated during the
Oligocene and Miocene.
Lineage Diversification Rates
The temporal method employed in END-EPI identified four nodes in the MCC with significant rate increases
(P < 0.05), all located in the early diversification of the
Noturus lineage (Fig. 1). The topological method employed in SymmeTREE identified significant rate variation among lineages (P = 0.0002–0.002) and two nearsignificant rate shifts (P = 0.07) in the MCC, one of which
was also identified by END-EPI. Summarized wholetree rate variation tests based on 1 × 104 samples from
the stationary distribution of the MC3 analysis were
of reduced significance (P = 0.07–0.03) with respect to
the tests based on the MCC, though they similarly implied or identified significant diversification rate hetero-
121
geneity. Although test statistics increased slightly in significance, including the unsampled taxa did not affect
the conclusions based on the original matrix and MCC.
The taxon-inclusion experiment did however identify
the node subtending all non-Ameiurus ictalurids as the
location of a significant diversification rate shift (P =
0.03). This clade received all of the unsampled taxa in
the experiment.
Reconstruction of lnMSL Evolution and Influence
on Species Richness
Convergence of the MCMC analyses in BayesTraits
was assessed by plotting the loglikelihood scores of
each sampled generation as time series and discarding
those beneath the asymptote (2.0 × 106 generations) as
burn-in. The BF (= 3.62) obtained from the comparison
of harmonic means of the marginal log likelihoods rejected the null hypothesis of a random walk in favor of
a directional model of evolution. Under the directional
model, mean ± standard deviations of the scaling parameters δ (0.88 ± 0.26), κ (0.70 ± 0.17), and λ (0.82 ±
0.10) suggested the majority of lnMSL evolution to have
taken place early in the lineage history, to have remained
fairly constant following those early changes, and to
be structured phylogenetically. Collectively, these values describe a punctuated model of evolution for MSL in
Ictaluridae.
Figure 2 shows scaled point estimates and 95% confidence intervals of the reconstructed ancestral MSLs.
Based on the WSP analysis, the ancestral ictalurid had
a mean MSL of 50.9 cm (with a 95% confidence interval of 27.8 to 93.1 cm), which is similar to the larger
species of modern Ameiurus. Similar ancestral conditions
were reconstructed for the common ancestors of the nonAmeiurus ictalurids (60.3 [29.7–122.4] cm) and of the lineage leading to Pylodictis and Noturus (68.1 [35.4–130.7]
cm). Although modern Ameiurus exhibit a range of MSLs,
the condition within the lineage was reconstructed as stable during the last 35 Ma, with the larger MSL of A. catus
reconstructed as autapomorphic in this early Miocene
lineage. Similarly, the large maximum size of Pylodictis olivaris was reconstructed as autapomorphic to this
early Eocene lineage rather than as an ancestral condition shared among other modern species with large
MSLs (Ictalurus furcatus: 165 cm; I. punctatus: 127 cm).
Within the Noturus lineage, MSL was reconstructed as
reducing rapidly to a value more typical of the modern
species early in their history and which changed rather
little after that, echoing the results of the MCMC analyses
in BayesTraits.
Least-squares regression through the origin identified
lnMSL as a nearly significant predictor of species richness (B = −0.470, SE = 0.251, t = −1.869, r 2 = 0.132,P =
0.07). Fifteen of 24 contrasts were negative, 8 were positive, and 1 was neutral (sign test: not significant, P =
0.21). The regression of contrast against node age (height)
was positive, indicating a decrease in lnMSL through
the history of Ictaluridae, corroborating the results of
BayesTraits and the WSP reconstruction. Additional tests
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SYSTEMATIC BIOLOGY
VOL. 57
FIGURE 1. Maximum credibility chronogram resulting from the combined samples of the stationary posterior distributions estimated in the
BEAST MCMC analysis. Branch lengths are in units of time and error bars represent the 95% highest posterior densities. Nodes labeled with
symbols were identified as the locations of significant (P < 0.05: filled circles and star) and nearly significant (P = 0.07: filled square and star)
diversification rate shifts in END-EPI and SymmeTREE, respectively. Lower bounds for the five constrained nodes are labeled in Ma. Inset shows
the plot of log lineage accumulation rate against the mean ocean temperature (climate) reconstruction of Zachos et al. (2001). Image of Ictalurus
furcatus reproduced from Etnier and Starnes (1993).
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HARDMAN AND HARDMAN—EVOLUTIONARY ANALYSIS OF BULLHEAD CATFISHES
123
FIGURE 2. Cladogram corresponding to the maximum credibility tree resulting from the BEAST MCMC analysis with posterior probabilities
displayed above branches and the proportion of 500 maximum likelihood bootstrap pseudoreplicates below (not shown if recovered in less than
0.50 of pseudoreplicates). Black silhouettes are scaled maximum standard lengths (MSLs) of the extant ictalurid fauna. Grey silhouettes are scaled
point estimates of ancestral MSLs with 95% confidence intervals in the accompanying shaded boxes. Filled circles, square, and star correspond
to the diversification rate shifts noted in Fig. 1 and text.
124
SYSTEMATIC BIOLOGY
suggested independence of the value of lnMSL and
species richness but significant variation in the relationship between lnMSL and species richness through time.
Correspondence of Diversification Rate
and Paleoclimatic Change
Figure 3 plots the rate and direction of MOT change
for the Cenozoic paleoclimate reconstruction of Zachos
et al. (2001) and the lnλ inferred from point estimates
VOL. 57
of node ages obtained from the BEAST MCMC analysis.
Although variation in the direction and rate of change
was noted for both reconstructions, the approaches employed to explore their correlation failed to reject the null
hypothesis of no association between the variables, either analyzed with respect to the basic observation of
paired changes (χ 2 = 2.96, df = 2, P = 0.227) or with respect to the rate of MOT change (Kendall’s τb = 0.065,
P = 0.529).
FIGURE 3. Time-series plots comparing the rate and direction of climate change and log per lineage accumulation rate over 58 one-millionyear intervals. Both chi-square and Kendall’s τb failed to reject the null hypothesis of no association between these two variables, but see text for a
discussion of the possible type II error. The abscissa on the upper plot represents no change in mean ocean temperature over 1 million years. The
smoothed line above zero represents climate warming, below represents climate cooling and its distance from zero describes the rate of change
in ◦ C/Ma. Filled symbols correspond to the diversification rate shifts noted in Fig. 1 and text.
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HARDMAN AND HARDMAN—EVOLUTIONARY ANALYSIS OF BULLHEAD CATFISHES
D ISCUSSION
Phylogeny
In evolutionary studies, phylogeny is of profound importance. In the majority of cases the branching pattern
is unknown but taxonomic congruence among phylogenies obtained from diverse data sources is considered
compelling evidence for their accuracy. In this study, results of the phylogenetic analysis were understandably
similar to earlier studies focused on subsets of the data
set analyzed here (Hardman and Page, 2003; Hardman,
2004; Near and Hardman, 2006; Egge and Simons, 2006).
Comparison with results obtained from morphological
data sets is restricted due to minimal overlap of taxon
sample, but with respect to intergeneric relationships,
significant differences have been observed (Hardman
and Page, 2003; Hardman, 2004). Previous phylogenetic
studies including exemplars of all ictalurid genera were
based on morphological characters polarized according
to their commonality in other fish groups; i.e., an implicit outgroup comparison (Lundberg, 1975, 1982, 1992).
Although J. G. Lundbergs’ dendrograms place Ictalurus sister to (Ameiurus (Pylodictis, Noturus)), the apparent conflict may be due to placement of the root rather
than significantly incongruent signal. Other morphologists have sampled catfishes broadly but did not include
exemplars of all epigean ictalurids (e.g., Mo, 1991; De
Pinna, 1998; Diogo, 2004) and are thus uninformative
with respect to intergeneric relationships. A recent survey of nuclear gene sequences among catfishes included
samples of the epigean ictalurids but failed to resolve
relationships among them convincingly (Sullivan et al.,
2006). Hence, we have no basis to consider the intergeneric resolution recovered here as inaccurate, though
it is without convincing MLBP support.
Within the convincingly monophyletic genera, relationships among species of Ameiurus were identical to
those reported by Hardman and Page (2003). Relationships among Noturus species were similar to those of
earlier studies based on the same or a subset of the data
analyzed here (Hardman, 2004; Burr et al., 2005; Near
and Hardman, 2006; Egge and Simons, 2006). Though
convincing support of the basal nodes in Noturus remains elusive, the pattern emerging from studies of
their phylogeny is that the subgenus Rabida is monophyletic, whereas Schilbeodes is not. Within Rabida, the
geographic distribution of several species groups corresponds to what might be expected under a peripheral
isolates model of speciation (Grady and LeGrande, 1992).
Species groups of Schilbeodes also correspond rather well
to geography: two species from the Coastal Plain, four
species from Atlantic Slope, and finally a clade with a
broad distribution throughout eastern North America.
The basal lineage of Noturus was recovered as the slender
madtom (N. exilis). This species has a rather large (536,600
km2 ; Grady and LeGrande, 1992) but fragmented distribution in streams of the Midwestern and southern
United States. Noturus exilis has been characterized as
having considerable genetic structure, with differences
suggesting diversification of the extant members of the
125
lineage to have taken place prior to or early in the Pleistocene (Hardy et al., 2002). Our estimate of the split between the lineage represented today by N. exilis and all
other Noturus is early Oligocene (mean 35.8; 95% HPD
26.8 to 41.9 Ma) during a period of significant (or nearly
significant) diversification rate increase (Figs. 1 to 3) and
dramatic climate cooling (Fig. 3).
Comparison of the Molecular Chronogram
and the Fossil Record
Although the comparative richness of the ictalurid fossil record (Lundberg, 1975, 1992) cannot be fully employed as constraints in divergence time estimation, the
temporal distribution of the unused fossils offers a check
of the chronology shown in Fig. 1.
Unfortunately, fossil Ameiurus species are difficult to
interpret in the present context because Hardman and
Page (2003) demonstrated significant phylogenetic conflict between the morphological data of Lundberg (1975,
1982, 1992) and the same sequences upon which our phylogeny and chronology are based. Thus, we were reluctant to use fossil species to provide indirect age minima
for their sister taxa according to morphology. However,
although no fossils of any extant Ameiurus species occur
outside of the estimates provided in Fig. 1, divergence
times suggest that the minima provided by the majority of Ameiurus fossils and those used to justify lower
bounds of lognormal priors considerably underestimate
lineage birth times.
The fossil record of Ictalurus (Lundberg, 1975, 1992) is
consistent with the DNA chronology in Figure 1. Fossils identified as I. punctatus have been found in middle
Miocene deposits of South Dakota and Nebraska (Lundberg, 1975, 1992) and were used to set a lower bound to
a lognormal prior specified in the UCLN MCMC analysis. These fossils predate the upper 95th percentile of the
HPD for the divergence time of I. punctatus and I. lupus
by at least 15 Ma. A possible explanation for this observation is that I. lupus represents a recently evolved species
that has diverged from an ancestral form that was morphologically indistinguishable from modern I. punctatus.
Thus, the Miocene fossils of I. punctatus correctly predate
the origin of I. lupus and characterize the evolution of I.
punctatus as one with a stable morphology similar to that
observed for P. olivaris (Lundberg, 1975, 1992).
We would like to stress that several species of Ictalurus
were not available for inclusion in this study. Though the
diversification rate experiment including these lineages
did not identify the node subtending all Ictalurus species
as the location of a significant shift in diversification rate,
their future analysis might offer some insight into the
processes of diversification in this larger-bodied clade in
Mexico and the southwestern United States.
Correspondence of Diversification Rate
and Paleoclimatic Change
Near et al. (2005) used a set of consistent fossil calibration points and mitochondrial and nuclear gene sequences to reconstruct the evolutionary chronology of
126
SYSTEMATIC BIOLOGY
sunfishes and basses (Centrarchidae) in Cenozoic North
America. According to a penalized likelihood analysis,
Near et al. (2005) estimated the root node age of centrarchids to be 33.59 ± 3.58–5.77 and suggested that the dramatic cooling of the climate at this time may have played
a role in their early diversification as well as the North
American ichthyofauna more generally. In line with the
hypothesis of a general response of the North American
biota, Webb and Opdyke (1995) characterized the evolution of land mammals as irregularly distributed in time
and tied to Cenozoic climate change.
Although the coincidence of the terminal Eocene event
and the significant (or nearly significant) increase in diversification rate of Noturus is striking (Fig. 1 inset; Fig.
3), our attempt to quantitatively examine a general association between diversification rate and climate change
did not detect a significant relationship. According to
the reconstruction of Zachos et al. (2001), the Cenozoic
climate was almost constantly changing, although the
rate and direction of change varied (Fig. 3). The significant shifts were tightly bounded in time, specific to early
branches of the Noturus lineage, and apparently coincided with the greatest period of climatic shift in the
Cenozoic. However, if a causal relationship exists between climate change and diversification in ictalurids,
why is it that only the Noturus lineage showed a significant response? The Ameiurus, Ictalurus, and Pylodictis
lineages were present at the time but (unless the fossil
record for these lineages is misleading) did not respond
significantly to the environmental change. Furthermore,
the dramatic cooling of the terminal Eocene event was
almost matched by an equally dramatic warming of the
climate in the Middle-Late Oligocene (Fig. 1 inset; Fig.
3) but no significant response in diversification rate was
noted.
We did not estimate the type II error rate (false negative) in the correspondence analysis of climate change
and diversification rate. Failure to reject the null may be
due to our use of point estimates of node ages that are,
in fact, inaccurate or that our arbitrary choice of onemillion-year measurement intervals is a poor reflection
of the time scale over which the effect operates. Additionally, diversification events may be the product of a
set of cumulative events that collectively create the circumstances under which the event can take place, and
division of that set into million-year slices effectively disrupts its detection. And although climate change appears
to have been the norm during the Cenozoic, warming
climates pose different changes to the environment than
does climate cooling so each climatic event likely posed
a different set of selective pressures (with different outcomes) that our rather coarse analysis failed to discriminate. Perhaps it was naı̈ve of us to look for a general
relationship between an extrinsic factor and diversification rate within a lineage history, though we might expect
it on the basis of phylogenetic constraint. Or perhaps the
response was only effective on ancestors with a particular body size and, therefore, different biology to the other
lineages. All these things (and many more) are possible, but accommodating the errors will decrease preci-
VOL. 57
sion and power to reject or reveal explicit evolutionary
phenomena.
We are left with an understanding that evolutionary
events operate on the standing diversity at a point in time
that is the sum of all prior events and their influence on
shaping its species, their communities and distributions.
In effect, no two evolutionary events within a lineage are
comparable and although significant diversification rate
shifts may be detected, their causes may be due to entirely different or ephemeral processes that operate only
under certain circumstances on a particular distribution
of extant diversity. Perhaps we might find general relationships across rather than within lineages, and running
multiple contemporary and sympatric clades through
the analytical procedure described here and by others
(Moore and Donoghue, 2007) might help to reveal a general model of macroevolutionary change in the Cenozoic,
if there is one to be found.
Interestingly, although Near et al. (2005) emphasized
the influence of the Eocene-Oligocene climatic shift on
North American freshwater fish diversification, most of
the extant centrarchid genera and species were reconstructed as late Oligocene, Miocene, and Pliocene in age.
So, perhaps the importance of the terminal Eocene event
as a driver of diversification has been overemphasized
and we should consider it more as an important period of
extinction rather than an important period of diversification; i.e., newly vacated niches being reoccupied rather
than increasing diversity within an already diverse system. Furthermore, based on the distribution of diversification events presented here and by Near et al. (2005),
we might find more evidence of an association between
climate change and diversification rate in the Oligocene
and Miocene.
Reconstruction of Ancestral MSLs and Correspondence
to Diversification
The MSLs of the early nodes in ictalurid history were
reconstructed as being ca. 50 to 60 cm, similar to those of
the larger modern Ameiurus. The much larger MSLs of
the extant Ictalurus furcatus (165.0 cm), Pylodictis olivaris
(155.0 cm), and I. punctatus (127.0 cm) were reconstructed
as autapomorphic increases from smaller ancestors, suggesting a homoplastic evolution of increasing body size
within the family. The Paleocene-Eocene Astephus were
similar in MSL (estimated 44.0 cm; Grande and Lundberg, 1988) to that estimated at the root node, suggesting
that the addition of proximal fossil lineages would have
little impact on its estimation and, therefore, support its
accuracy (Oakley and Cunningham, 2000; Finarelli and
Flynn, 2006). Additionally, the MSLs of extant Cranoglanis (43.0 cm; Zheng, 1990) further reinforce the ancestral MSL of Ictaluridae as an approximately half-meter
fish. The positive correlation of body size and dispersal
is a well known phenomenon (Ware, 1978; Bernatchez
and Dodson, 1987) and a half-meter ancestral ictalurid
could presumably navigate the physical and physiological barriers met in a dispersal route through a Beringian
land bridge during the Late Cretaceous or Early Tertiary
(Hardman, 2005).
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HARDMAN AND HARDMAN—EVOLUTIONARY ANALYSIS OF BULLHEAD CATFISHES
With respect to the species richness discrepancy observed between Pylodictis and Noturus, the increased
MSL of P. olivaris (155.0 cm) from an ancestral condition of 68.1 (35.4–122.4) cm could explain the failure of
this lineage to diversify. The combination of a preference
for habitats that typically connect adjacent drainages in
times of abundant rainfall coupled with its breathtaking dispersal within and among seeded systems (Guier
et al., 1981; Kwak et al., 2004; Brown et al.,2005) likely
maintains and promotes gene flow among populations
of P. olivaris and offers an explanation of the species’
morphological homogeneity over time (Lundberg, 1975,
1992).
A larger MSL for the ancestral Noturus than shown
by the majority of extant species also makes sense given
the large distribution of a genus that today is composed
of rather small and fragmented ranges of many smallbodied species. Of the Noturus species with large distributions, N. gyrinus is atypical for the genus in that it
is commonly found in lowland habitats through which
its dispersal is presumably enhanced (Taylor, 1969; Page
and Burr, 1991). Noturus flavus is the largest member
of the genus at 31.0 cm, so its range can be explained
in terms of a larger MSL. Noturus eleutherus, N. miurus, and N. stigmosus are all less than 15.0 cm but are
found in large streams through which they presumably
enjoy dispersal throughout the Ohio and Mississippi
drainages. The low genetic differentiation (Hardman,
2004) and large range of the Atlantic Slope N. insignis
(MSL of 15.0 cm) is anomalous and a subject for further
study.
CONCLUSIONS
If we ignore our concerns and let the results tell their
story, the analyses of Ictaluridae found diversification
rate to have varied significantly during the Cenozoic and
significant (or nearly significant) increases were implied
for early nodes in the Noturus lineage. The evolution of
lnMSL followed a directional (decreasing) model and
was found to be a nearly significant predictor of species
richness, with clades composed of small species being
proportionally more species rich than expected under a
null model. The chronology of diversification describes
the origins of the extant genera during the Paleocene
and early Eocene and the majority of extant species to
be Oligocene and Miocene in age. Climate change did
not significantly affect diversification rate throughout
the history of the lineage.
We estimated the maximum standard length of the ictalurid ancestor to be approximately 50 cm, comparable
to Eocene ictalurids (Astephus) and similar to modern
sizes of Ameiurus and the Asian sister taxon Cranoglanis.
Based on the properties of modern fishes of similar size,
the hypothetical ancestor would be suitably sized to disperse from Asia into North America through freshwater
systems of Beringia (Hardman, 2005).
The covariation of increasing size, large distribution,
and low diversity appears to be a general one shown by
127
Pylodictis olivaris, Ictalurus furcatus, and I. punctatus. All
three species regularly grow well over a meter and have
large natural distributions. Additionally, all three appear
to be rather ancient species with conservative morphologies that have independently increased their maximum
standard lengths from smaller ancestors, as implied by
the fossil record and reconstructions presented here. Presumably, the common diversification process of peripheral isolation fails to operate when species evolve large
body sizes and, consequently, expand their distributions
within which dispersal and migration maintain or increase gene flow. The small-bodied lineage, on the other
hand, has experienced a diversification rate significantly
higher than its larger cousins and the patchy distributions of many modern Noturus suggest a separate set of
evolutionary processes have applied to this clade.
ACKNOWLEDGMENTS
Special thanks to B. Moore and J. Lundberg for their detailed,
thoughtful, and tremendously helpful comments on an earlier version
of this paper. Also, J. Knouft, L. Page, and A. Summers provided excellent counsel on macroevolutionary matters, North American freshwater fishes, and their thoughts on the importance of body size. N. Isaac,
A. Meade, B. Moore, and A. Rambaut provided software and technical
support. We thank H. Henttonen for providing logistic and informatics
support during the course of this project. M.H. was supported by the
All Catfish Species Inventory (NSF: DEB 0315963) and L.H. by a Finnish
Academy Postdoctoral Research Grant (no. 108372; Wickström et al.,
2005).
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First submitted 28 May 2007; reviews returned 16 August 2007;
final acceptance 14 November 2007
Associate Editor: Allan Baker