A general relationship between rates of diversification and rates of morphological evolution may be expected for several reasons. For example, the ecological theory of adaptive radiation predicts accelerated rates of speciation associated with divergence in ecologically relevant phenotypic traits (e.g. Schluter 2000
), at least at some points in the radiation process. The hypothesis of punctuated equilibrium (e.g. Gould & Eldredge 1977
) predicts that most evolutionary change occurs at speciation events, which might also lead to a correlation between rates of species diversification and morphological change (e.g. Ricklefs 2006a
; Bokma 2008
), in some cases (e.g. if diversification rates vary among clades). A previous study on species diversity and morphological disparity in birds (Ricklefs 2004
) also implied that these rates were correlated. However, simulations suggested that morphological variance and species richness of clades should generally be correlated (Purvis 2004
; Ricklefs 2006a
), due to the dependence of both variables on clade age (i.e. diversity and disparity should be high in old clades, even if rates of species diversification and morphological evolution are similar across clades).
Despite these expectations, our results show that rates of morphological diversification and species diversification are not significantly correlated in plethodontid salamanders. For example, the clade with the highest rate of species diversification (Bolitoglossa subgenus Eladinea) has unexceptional rates of morphological evolution, and the clade with the highest rate of change in size and second highest rate of shape evolution (Eurycea) has only a moderate rate of species diversification (). Our results also suggest that morphological disparity may not always be an adequate proxy for rates of change, as we found a relationship between standard measures of disparity and rates of size change, but not shape change, in plethodontids (though rates of shape change are related to shape disparity). This result reinforces the need to examine rates of phenotypic change and species diversification in a phylogenetic context.
In theory, the lack of a significant relationship between rates of species diversification and morphological evolution might be explained by one of several methodological artefacts, but this seems unlikely. First, this correlation might exist, but the power of our study may be too weak to detect it (e.g. too few clades, not enough variation among them). However, rates of size and shape evolution were sufficiently variable to show significant associations with other variables (i.e. disparity, each other), and rates of species diversification also show significant variation among clades (see below). Second, our sampling of species within clades, although extensive (190), is not complete. However, our estimates of species diversification rates do incorporate all described species within each clade, regardless of whether they are included in our phylogenies. Incomplete sampling could affect estimates of morphological rates, but we also find no significant relationship between species diversification and morphological evolution when we estimate both rates only from species included in the phylogeny (table 2s in the electronic supplementary material). Additionally, the broad morphological overlap between taxa included in our phylogeny and those not included suggests that patterns of morphological variation we observed were not biased by excluding these taxa. Our results are also robust to alternative divisions of plethodontids into clades (electronic supplementary material). We acknowledge that our conclusions about morphological evolution are confined to those characters that we measured; namely body size and the relative proportions of head, trunk, limbs and tail. Although these characters describe dramatic variation in body size and shape, other traits are not included, such as modes of tongue projection (e.g. Lombard & Wake 1986
), cranial morphology (e.g. Wake 1966
; Adams 2004
; Adams et al. 2007
) and foot morphology (e.g. Alberch 1981
; Jaekel & Wake 2007
). However, even if we have neglected to include a ‘key innovation’ trait that explains variation in diversification rates between clades, our goal here is to determine whether clades with accelerated diversification rates also have accelerated rates of within-clade morphological evolution. Although morphologically cryptic species have been documented in most plethodontid clades (and represent obvious decoupling of species diversification and morphological change), these do not seem to explain the pattern either. For example, many morphologically cryptic species are known in Eurycea
(Kozak et al. 2006b
), yet this genus has high rates of morphological evolution but not species diversification (). If cryptic species explained the lack of relationship, one would expect high rates of species diversification accompanied by low rates of morphological change.
Given our finding of no significant relationship between species diversification and morphological evolution, what might explain patterns of variation in these variables? Some variation in species diversification rates may be explained by the latitudinal position of clades. A relationship between low latitudes and high diversification rates has been found in many previous studies, including salamanders and frogs (Wiens 2007
), birds (Cardillo 1999
; Cardillo et al. 2005
; Ricklefs 2006b
), butterflies (Cardillo 1999
) and palms (Svenning et al. 2008
). In plethodontids, rates of diversification are significantly higher in tropical clades (Bolitoglossinae, clades 9–15) than temperate clades (Plethodontinae, clades 1–6; Spelerpinae, clades 7–8), based on a t
-test of data in (d.f.=13; p
=0.02; but note that the tropical clades are all closely related). The tropical bolitoglossines are the only primarily tropical clade of salamanders and collectively have the highest species diversification rate of any major salamander clade (Wiens 2007
). This pattern may be related to higher extinction rates in temperate clades or higher speciation rates in tropical clades. Regardless of the rate of diversification, speciation in tropical salamanders seems to have a strong climatic component; sister species tend to occur in different climatic environments associated with different elevations, whereas temperate sister species tend to occur in similar environments (Kozak & Wiens 2007
). If speciation occurs primarily through geographic isolation related to climatic factors, there may be little reason to expect morphological divergence to generally accompany speciation (unless climate-related factors impose selection on body form). Similarly, reproductive isolation may be promoted by divergence in courtship pheromones (e.g. Palmer et al
), which may not lead to morphological differences among species.
One might expect higher species diversification rates to be related to the invasion of morphospace not occupied by other plethodontid clades, given the idea that a clade will tend to constrain the diversification of sympatric, phenotypically similar clades (e.g. Schluter 2000
). However, this prediction is not supported in plethodontids (see also Kozak et al. in press
). In the traits we examined, most plethodontid clades show surprisingly similar patterns of morphological variation; most clades exhibit similar body shape (PC2) and even a similar range of body sizes (PC1), and differences between species within clades seem to mostly involve sliding up and down this range of body sizes (b
). Only a few clades have deviated from this pattern. The most obvious exception is Oedipina
), which shows little overlap with other clades in morphological space (due to an elongate tail and short limbs). However, despite its unusual morphology, Oedipina
shows only moderate rates of species diversification (). The Pseudoeurycea
clade has also invaded a portion of morphospace similar to Oedipina
, and has high rates of species diversification, size change and shape change. However, only three species of the Pseudoeurycea
clade have this worm-like morphology (i.e. the three species of Lineatriton
), and most species diversification has instead involved species with more typical body forms (a
). In summary, most species diversification in plethodontids has occurred in a relatively small region of morphospace, a region that is shared by most clades (a
). Similarly, Ricklefs (2005)
found that clades of passerine birds with limited species richness tended to be in the periphery of multivariate morphospace, relative to more diverse clades.
Patterns of species diversification also appear generally unrelated to allopatry of clades, with one important exception. Notably, the highest rates of species diversification in plethodontids are in the subgenus Eladinea
(), which occurs primarily in South America and is mostly allopatric with respect to other plethodontid clades (Wiens et al. 2007
). However, other plethodontid clades are sympatric with one or more other clades, despite considerable variation in diversification rates. For example, the Plethodon glutinosus
group has a diversification rate approaching that of Eladinea
(), but is microsympatric with up to five other plethodontid clades in many localities in eastern North America (clades 1, 4, 5, 7, 8; Petranka 1998
). There is also extensive sympatry between clades of tropical bolitoglossines (e.g. Chiropterotriton
in Mexico; Bolitoglossa
in Central America; Wake 1987
). Intriguingly, we see no obvious shifts in morphospace associated with either allopatry or sympatry of these clades (a
We also found that rates of size and shape evolution are strongly correlated. To our knowledge no previous studies have tested for this relationship. Why should these variables be correlated? One hypothesis is that if ecomorphs differ in both size and shape (e.g. West Indian Anolis
lizards; Losos et al. 1998
), then rates of size and shape evolution will be coupled and will depend on the rate at which ecomorphs evolve in each clade. Shared allometric relationships among species within clades (i.e. similar shapes evolve when similar sizes evolve) might also cause these rates to be correlated. Alternately, within a given clade there could be rapid size evolution in one subclade and rapid shape evolution in another; this could lead to high rates of evolution in both traits among clades, even without a correlation within clades. However, we also found a general relationship between size and shape evolution at the species level, which parallels the correlated patterns of rate evolution among clades. Although much morphological evolution in plethodontids seems to involve clades with similar body shapes undergoing shifts in body size, at least in some clades, shifts in body size are also accompanied by changes in body shape.
In this study, we present the first direct test of whether rates of species diversification and morphological evolution are correlated across clades, and find no significant relationship, despite theoretical and empirical expectations. The generality of these results will need to be tested in other groups of organisms, preferably using similar phylogeny-based approaches. Our results imply that speciation in plethodontids typically is not accompanied by extensive phenotypic divergence, but may be associated instead with other factors that bear more directly on reproductively isolating populations, such as climatic factors limiting geographic ranges. Our results also suggest that patterns of morphological evolution in body form are highly redundant across plethodontid clades, with most clades sharing similar general body form and diverging primarily in body size, regardless of their rates of species diversification or the presence of other sympatric clades.