Disparity and Evolutionary Rate Do Not Explain Diversity Patterns in Muroid Rodents (Rodentia: Muroidea)

A positive correlation between diversity and disparity/evolutionary rate is predicted by multiple evolutionary theories. However, recent empirical studies in various taxa do not always find such an association. Similarly, we find no correlation between these two levels of variation, based on cranial morphometric data and molecular phylogenetic data from 317 muroid rodent species and dipodoid outgroups, analyzed using three-dimensional geometric morphometrics. This disassociation was found using both phylogenetic and non-phylogenetic approaches, indicating that an increase in clade richness is not necessarily followed by an increase in morphological divergence and vice versa. Furthermore, the distribution of muroid families in morphospace is highly overlapping suggesting greater variation within than between clades. Taken together with the observation that families with the most distinctive cranial morphologies (nesomyids, dipodids, and spalacids) are the least diverse, indicates that evolution of new cranial morphologies may not play an important role in the diversification of muroid rodents.     

Ecomorphological diversification following continental colonization in muroid rodents (Rodentia: Muroidea)

The emergence of exceptionally diverse clades is often attributed to ecological opportunity. For example, the exceptional diversity in the most diverse superfamily of mammals, muroid rodents, has been explained in terms of multiple independent adaptive radiations. If multiple ecological opportunity events are responsible for generating muroid diversity, we expect to find evidence of these lineages ecologically diversifying following dispersal into new biogeographical areas. In the present study, we tested the trait‐based predictions of ecological opportunity using data on body size, appendages, and elevation in combination with previously published data on biogeographical transitions and a time‐calibrated molecular phylogeny. We identified weak to no support of early ecological diversification following the initial colonizations of all continental regions, based on multiple tests, including node height tests, disparity through time plots, evolutionary model comparison, and Bayesian analysis of macroevolutionary mixtures. Clades identified with increased diversification rates, not associated with geographical transitions, also did not show patterns of phenotypic divergence predicted by ecological opportunity, which suggests that phylogenetic diversity and phenotypic disparity may be decoupled in muroids. These results indicate that shifts in diversification rates and biogeographically‐mediated ecological opportunity are poor predictors of phenotypic diversity patterns in muroids.     

Trait evolution rates shape continental patterns of species richness in North America's most diverse angiosperm genus (Carex,Cyperaceae)

Ecological opportunity has been associated with increases in diversification rates across the tree of life. Under an ecological diversification model, the emergence of novel environments is hypothesized to promote morpho- and ecospace evolution. Whether this model holds at the clade level within the most species-rich angiosperm genus found in North America (Carex, Cyperaceae) is yet to be tested. Recent works demonstrate a temporal coupling of climate cooling and widespread colonization of Carex in North America, implicating ecological diversification. In addition, research has consistently found asymmetric patterns of lineage-level diversification in the genus. Why does variation in clade sizes exist in the genus? Is ecological diversification involved? In this study, we tested whether rates of morphological and ecological trait evolution are correlated with clade-level species richness in Carex of North America north of Mexico. We constructed a phylogeny of 477 species—an almost complete regional sample. We estimated rates of evolution of morphological traits, habitat, and climatic niche and assessed whether differences in rates of evolution correlate with species richness differences in replicate non-nested sister clades. Our work demonstrates significant positive correlations between climatic niche rates, habitat and reproductive morphological evolution, and species richness. This coupling of trait and niche evolution and species richness in a diverse, continental clade sample strongly suggests that the ability of clades to explore niche and functional space has shaped disparities in richness and functional diversity across the North American flora region. Our findings highlight the importance of the evolutionary history of trait and niche evolution in shaping continental and regional floras.     

Ecological specialization and morphological diversification in Greater Antillean boas

Colonization of islands can dramatically influence the evolutionary trajectories of organisms, with both deterministic and stochastic processes driving adaptation and diversification. Some island colonists evolve extremely large or small body sizes, presumably in response to unique ecological circumstances present on islands. One example of this phenomenon, the Greater Antillean boas, includes both small (<90 cm) and large (4 m) species occurring on the Greater Antilles and Bahamas, with some islands supporting pairs or trios of body‐size divergent species. These boas have been shown to comprise a monophyletic radiation arising from a Miocene dispersal event to the Greater Antilles, though it is not known whether co‐occurrence of small and large species is a result of dispersal or in situ evolution. Here, we provide the first comprehensive species phylogeny for this clade combined with morphometric and ecological data to show that small body size evolved repeatedly on separate islands in association with specialization in substrate use. Our results further suggest that microhabitat specialization is linked to increased rates of head shape diversification among specialists. Our findings show that ecological specialization following island colonization promotes morphological diversity through deterministic body size evolution and cranial morphological diversification that is contingent on island‐ and species‐specific factors.     

Tightly congruent bursts of lineage and phenotypic diversification identified in a continental ant radiation

Adaptive diversification is thought to be shaped by ecological opportunity. A prediction of this ecological process of diversification is that it should result in congruent bursts of lineage and phenotypic diversification, but few studies have found this expected association. Here, we study the relationship between rates of lineage diversification and body size evolution in the turtle ants, a diverse Neotropical clade. Using a near complete, time‐calibrated phylogeny we investigated lineage diversification dynamics and body size disparity through model fitting analyses and estimation of per‐lineage rates of cladogenesis and phenotypic evolution. We identify an exceptionally high degree of congruence between the high rates of lineage and body size diversification in a young clade undergoing renewed diversification in the ecologically distinct Chacoan biogeographical region of South America. It is likely that the region presented turtle ants with novel ecological opportunity, which facilitated a nested burst of diversification and phenotypic evolution within the group. Our results provide a compelling quantitative example of tight congruence between rates of lineage and phenotypic diversification, meeting the key predicted pattern of adaptive diversification shaped by ecological opportunity.     

ECOLOGICAL CAUSES OF DECELERATING DIVERSIFICATION IN CARNIVORAN MAMMALS

Clade diversification is a central topic in macroevolutionary studies. Recently, it has been shown that diversification rates appear to decelerate over time in many clades. What causes this deceleration remains unclear, but it has been proposed that competition for limited resources between sympatric, ecologically similar species slows diversification. Employing carnivoran mammals as a model system, we test this hypothesis using a comprehensive time‐calibrated phylogeny. We also explore several conceptually related explanations including limited geographic area and limited rates of niche evolution. We find that diversification slowdowns are strong in carnivorans. Surprisingly, these slowdowns are independent of geographic range overlap between related species and are also decoupled from rates of niche evolution, suggesting that slowdowns are unrelated to competition and niche filling. When controlling for the effects of clade diversity, diversification slowdowns appear independent of geographic area. There is a significant effect of clade diversity on diversification slowdowns, but simulations show that this relationship may arise as a statistical artifact (i.e., greater clade diversity increases the ability of the gamma statistic to refute constant diversification). Overall, our results emphasize the need to test hypotheses about the causes of diversification slowdowns with ecological data, rather than assuming ecological processes from phylogenies alone.     

Sperm morphology in the Malagasy rodents (Muroidea: Nesomyinae)

The morphology of the spermatozoon of representative species of the subfamily Nesomyinae (Muroidea: Nesomyidae), a monophyletic group of rodents endemic to Madagascar, was examined by light and electron microscopy to determine the sperm head shape and tail length across the species. Marked interspecific differences were found to occur in both the form of the sperm head and length of the tail. The species that possess a sperm head with an apical hook, which largely contains acrosomal material, generally displayed longer sperm tails, and a species with a spatulate sperm head had the shortest tail. The association between sperm head shape and tail length mirrors that previously found in Eurasian and Australasian murine rodents. Thus, the repeated association between sperm head shape and tail length across these groups of muroid rodents clearly indicates a functional relationship between these two features. A comparison of sperm morphology of the nesomyines to that of related muroid rodents on the mainland of Africa suggests that the possession of an apical hook is the ancestral condition. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Primary controls on species richness in higher taxa

The disparity in species richness across the tree of life is one of the most striking and pervasive features of biological diversity. Some groups are exceptionally diverse, whereas many other groups are species poor. Differences in diversity among groups are frequently assumed to result from primary control by differential rates of net diversification. However, a major alternative explanation is that ecological and other factors exert primary control on clade diversity, such that apparent variation in net diversification rates is a secondary consequence of ecological limits on clade growth. Here, I consider a likelihood framework for distinguishing between these competing hypotheses. I incorporate hierarchical modeling to explicitly relax assumptions about the constancy of diversification rates across clades, and I propose several statistics for a posteriori evaluation of model adequacy. I apply the framework to a recent dated phylogeny of ants. My results reject the hypothesis that net diversification rates exert primary control on species richness in this group and demonstrate that clade diversity is better explained by total time-integrated speciation. These results further suggest that it may not possible to estimate meaningful speciation and extinction rates from higher-level phylogenies of extant taxa only.     

Climatic niche conservatism and ecological opportunity in the explosive radiation of arvicoline rodents (Arvicolinae,Cricetidae)

Climatic niche conservatism shapes patterns of diversity in many taxonomic groups, while ecological opportunity (EO) can trigger rapid speciation that is less constrained by the amount of time a lineage has occupied a given habitat. These two processes are well studied, but limited research has considered their joint and relative roles in shaping diversity patterns. We characterized climatic and biogeographic variables for 102 species of arvicoline rodents (Arvicolinae, Cricetidae), testing the effects of climatic niche conservatism and EO on arvicoline diversification as lineages transitioned between biogeographic regions. We found that the amount of time a lineage has occupied a precipitation niche is positively correlated with diversity along a precipitation gradient, suggesting climatic niche conservatism. In contrast, shift in diversification rate explained diversity patterns along a temperature gradient. Our results suggest that an indirect relationship exists between temperature and diversification that is associated with EO as arvicoline rodents colonized warm Palearctic environments. Climatic niche conservatism alone did not fully explain diversity patterns under density‐dependence, highlighting the additional importance of EO‐related processes in promoting the explosive radiation in arvicoline rodents and shaping diversity pattern among biogeographic regions and along climatic gradients.     

Biotic and abiotic factors driving the diversification dynamics of Crocodylia

Species diversity patterns are governed by complex interactions among biotic and abiotic factors over time and space, but are essentially the result of the diversification dynamics (differential speciation and extinction rates) over the long-term evolutionary history of a clade. Previous studies have suggested that temporal variation in global temperature drove long-term diversity changes in Crocodylia, a monophyletic group of large ectothermic organisms. We use a large database of crocodylian fossil occurrences (192 spp.) and body mass estimations, under a taxic approach, to characterize the global diversification dynamics of crocodylians since the Cretaceous, and their correlation with multiple biotic and abiotic factors in a Bayesian framework. The diversification dynamic of crocodylians, which appears to have originated in the Turonian (c. 92.5 Ma), is characterized by several phases with high extinction and speciation rates within a predominantly low long-term mean rate. Our results reveal long-term diversification dynamics of Crocodylia to be a highly complex process driven by a combination of biotic and abiotic factors which influenced the speciation and extinction rates in dissimilar ways. Higher crocodylian extinction rates are related to low body mass disparity, indicating selective extinctions of taxa at both ends of the body mass spectrum. Speciation rate slowdowns are noted when the diversity of the clade is high and the warm temperate climatic belt is reduced. Our finding supports the idea that temporal variations of body mass disparity, self-diversity, and the warm climate belt size provided more direct mechanistic explanations for crocodylian diversification than do proxies of global temperature.     

Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions

Diversification rate is one of the most important metrics in macroecological and macroevolutionary studies. Here I demonstrate that diversification analyses can be misleading when researchers assume that diversity increases unbounded through time, as is typical in molecular phylogenetic studies. If clade diversity is regulated by ecological factors, then species richness may be independent of clade age and it may not be possible to infer the rate at which diversity arose. This has substantial consequences for the interpretation of many studies that have contrasted rates of diversification among clades and regions. Often, it is possible to estimate the total diversification experienced by a clade but not diversification rate itself. I show that the evidence for ecological limits on diversity in higher taxa is widespread. Finally, I explore the implications of ecological limits for a variety of ecological and evolutionary questions that involve inferences about speciation and extinction rates from phylogenetic data.     

Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences

The rodent family Muridae is the single most diverse family of mammals with over 1300 recognized species. We used DNA sequences from the first exon ( approximately 1200bp) of the IRBP gene to infer phylogenetic relationships within and among the major lineages of muroid rodents. We included sequences from every recognized muroid subfamily except Platacanthomyinae and from all genera within the endemic Malagasy subfamily Nesomyinae, all recognized tribes of Sigmodontinae, and a broad sample of genera in Murinae. Phylogenetic analysis of the IRBP data suggest that muroid rodents can be sorted into five major lineages: (1) a basal clade containing the fossorial rodents in the subfamilies Spalacinae, Myospalacinae, and Rhizomyinae, (2) a clade of African and Malagasy genera comprising the subfamilies Petromyscinae, Mystromyinae, Cricetomyinae, Nesomyinae, and core dendromurines, (3) a clade of Old World taxa belonging to Murinae, Otomyinae, Gerbillinae, Acomyinae, and Lophiomyinae, (4) a clade uniting the subfamilies Sigmodontinae, Arvicolinae, and Cricetinae, and (5) a unique lineage containing the monotypic Calomyscinae. Although relationships among the latter four clades cannot be resolved, several well-supported supergeneric groupings within each are identified. A preliminary examination of molar tooth morphology on the resulting phylogeny suggests the triserial murid molar pattern as conceived by evolved at least three times during the course of muroid evolution.     

ADAPTIVE RADIATION AND ECOLOGICAL DIVERSIFICATION OF SULAWESI'S ANCIENT LAKE SHRIMPS

Ancient lakes are natural laboratories for the study of adaptive radiation. Recently, two lake systems on the Indonesian island Sulawesi have emerged as promising new model systems. A species flock of atyid freshwater shrimps in the Malili lake system comprises 15 colorful endemic taxa. Mitochondrial DNA data suggest two independent colonizations by riverine ancestors. Only one colonization event led to subsequent radiation into 14 species, while the second clade comprises just one species. The vast majority of species (n= 12) are habitat specialists, which are confined to the larger Malili clade and include all taxa with species‐specific color patterns and a restricted distribution within the five connected Malili lakes. Morphological, genetic, and ecological data are consistent with the existence of an adaptive radiation in the Malili lakes, involving the habitat‐specific diversification of trophic morphology. In addition to testing criteria for the recognition of an adaptive radiation, an ancestral state reconstruction reveals an equal probability for either a riverine generalist or a lacustrine specialist as ancestor of the large Malili clade, which is interpreted as indicative of an early stage of habitat specialization within this radiation. Finally, our results suggest that species diversification may have been primarily driven by ecological specialization and allopatric speciation.     

Unravelling the distinctive craniomandibular morphology of the Plio-Pleistocene Eumysops in the evolutionary setting of South American octodontoid rodents (Hystricomorpha)

Echimyidae is a species-rich clade of Neotropical rodents, which diversified in association with forested biomes. Since the late Miocene, a few lineages from southern South America have been adapted to open environments. Eumysops is one of these southern echimyids, and its peculiar craniomandibular morphology has been assumed to be a result of adaptation to open environments. We performed a geometric morphometric analysis of craniomandibular shape variation to explore whether, as suspected, Eumysops is divergent from other echimyids and octodontoids. In addition, we explored whether deterministic factors driven by different ecological dimensions can explain the diversification of shape among octodontoids. We found that craniomandibular shape variation in octodontoids was related to ecological variables. Comparing competing evolutionary models suggested that the input of selective factors play a key role in octodontoid craniomandibular shape diversification; habitat and habits were found to be the most influential factors. In the analysed morphospaces, Eumysops was located distant from other echimyids due to its distinctive traits, especially wide and posteriorly displaced orbits, and related low craniomandibular joint. Divergent orbits and resulting wider panoramic vision support the interpretation of Eumysops as an open-habitat specialist echimyid. But what is more relevant, is that Eumysops occupied a sector of the octodontoid cranial morphospace not filled by living representatives; this highlights the contribution of fossils in providing key information on the specialization boundaries explored by a clade throughout its history.     

Evolution of the spermatozoon in muroid rodents

In the rodent superfamily Muroidea, a model for the evolution of sperm form has been proposed in which it is suggested that a hook-shaped sperm head and long tail evolved from a more simple, nonhooked head and short tail in several different subfamilies. To test this model the shape of the sperm head, with particular emphasis on its apical region, and length of sperm tail were matched to a recent phylogeny based on the nucleotide sequence of several protein-coding nuclear genes from 3 families and 10 subfamilies of muroid rodents. Data from the two other myomorph superfamilies, the Dipodoidea and kangaroo rats in the Geomyoidea, were used for an outgroup comparison. In most species in all 10 muroid subfamilies, apart from in the Murinae, the sperm head has a long rostral hook largely composed of acrosomal material, although its length and cross-sectional shape vary across the various subfamilies. Nevertheless, in a few species of various lineages a very different sperm morphology occurs in which an apical hook is lacking. In the outgroups the three species of dipodid rodents have a sperm head that lacks a hook, whereas in the heteromyids an acrosome-containing apical hook is present. It is concluded that, as the hook-shaped sperm head and long sperm tail occur across the muroid subfamilies, as well as in the heteromyid rodents, it is likely to be the ancestral condition within each of the subfamilies with the various forms of nonhooked sperm heads, that are sometimes associated with short tails, being highly derived states. These findings thus argue against a repeated evolution in various muroid lineages of a complex, hook-shaped sperm head and long sperm tail from a more simple, nonhooked sperm head and short tail. An alternative proposal for the evolution of sperm form within the Muroidea is presented in the light of these data.     

Key evolutionary innovations and their ecological mechanisms

Explanations for taxonomic diversity in a particular clade often implicate evolutionary innovations, possessed by members of the clade, that are thought to have favoured diversification. We review such “key innovation”; hypotheses, the ecological mechanisms involved, and potential tests of such hypotheses.

Key innovation hypotheses can be supported by evidence of ecological mechanism and by comparative tests. We argue that both are necessary for convincing support. In fact, few key innovation hypotheses are currently backed by either one.

We group ecological mechanisms of diversification in three major classes. Diversification may be spurred by innovations that: I) allow invasion of new adaptive zones; II) increase fitness, allowing one clade to replace another; or III) increase the propensity for reproductive or ecological specialization. Key innovations in different classes are likely to produce different evolutionary patterns, and therefore may be supported by different kinds of ecological evidence.     

Vive le difference! Sexual dimorphism and adaptive patterns in lizards of the genus Anolis

The repeated, convergent evolution of body shape and microhabitat use in Greater Antillean lizards of the genus Anolis (anoles) provides compelling evidence of the importance of microhabitat specialization in shaping morphology. Interestingly, sexual dimorphism is also extensive, with males and females differing in body size as well as in shape. It is important to note that the components of shape analyzed in these studies is related to locomotion and are size-adjusted, including: relative limb and body lengths and mass of the body. Numbers of lamellae were also used and these do not vary with size. Furthermore, dimorphism in both size and shape differs by habitat type. Thus, does functionally-relevant sexual dimorphism imply that one sex is the "ecological" sex, with the other being maladapted to it's environment? Alternatively, sexual dimorphism may interact with adaptive diversification. Different classes of individuals within a species may act as separate ecological units if they play ecologically different roles. Here, I reanalyze a data set of morphological data for 15 species of Puerto Rican and Jamaican Anolis, which represent two largely independent adaptive radiations of lizards. I test for concordance between size and shape dimorphism and microhabitat (ecomorph) type, and for "parallel" patterns of sexual dimorphism among species. I integrate these results and, in the light of previous research, evaluate the relative influence that larger-scale ecological patterns have on sexual dimorphism, as well as the influence of sexual dimorphism on community structuring. I conclude that the presence of ecologically-relevant dimorphism may in fact increase the adaptive diversity present within a community.     

The role of ecological opportunity in shaping disparate diversification trajectories in a bicontinental primate radiation

Exceptional species and phenotypic diversity commonly are attributed to ecological opportunity (EO). The conventional EO model predicts that rates of lineage diversification and phenotypic evolution are elevated early in a radiation only to decline later in response to niche availability. Foregut fermentation is hypothesized to be a key innovation that allowed colobine monkeys (subfamily Colobinae), the only primates with this trait, to successfully colonize folivore adaptive zones unavailable to other herbivorous species. Therefore, diversification rates also are expected to be strongly linked with the evolution of traits related to folivory in these monkeys. Using dated molecular phylogenies and a dataset of feeding morphology, I test predictions of the EO model to evaluate the role of EO conferred by foregut fermentation in shaping the African and Asian colobine radiations. Findings from diversification methods coupled with colobine biogeographic history provide compelling evidence that decreasing availability of new adaptive zones during colonization of Asia together with constraints presented by dietary specialization underlie temporal changes in diversification in the Asian but not African clade. Additionally, departures from the EO model likely reflect iterative diversification events in Asia.     

AN ADAPTIVE RADIATION OF FROGS IN A SOUTHEAST ASIAN ISLAND ARCHIPELAGO

Living amphibians exhibit a diversity of ecologies, life histories, and species‐rich lineages that offers opportunities for studies of adaptive radiation. We characterize a diverse clade of frogs (Kaloula, Microhylidae) in the Philippine island archipelago as an example of an adaptive radiation into three primary habitat specialists or ecotypes. We use a novel phylogenetic estimate for this clade to evaluate the tempo of lineage accumulation and morphological diversification. Because species‐level phylogenetic estimates for Philippine Kaloula are lacking, we employ dense population sampling to determine the appropriate evolutionary lineages for diversification analyses. We explicitly take phylogenetic uncertainty into account when calculating diversification and disparification statistics and fitting models of diversification. Following dispersal to the Philippines from Southeast Asia, Kaloula radiated rapidly into several well‐supported clades. Morphological variation within Kaloula is partly explained by ecotype and accumulated at high levels during this radiation, including within ecotypes. We pinpoint an axis of morphospace related directly to climbing and digging behaviors and find patterns of phenotypic evolution suggestive of ecological opportunity with partitioning into distinct habitat specialists. We conclude by discussing the components of phenotypic diversity that are likely important in amphibian adaptive radiations.     

DO FRESHWATER FISHES DIVERSIFY FASTER THAN MARINE FISHES? A TEST USING STATE‐DEPENDENT DIVERSIFICATION ANALYSES AND MOLECULAR PHYLOGENETICS OF NEW WORLD SILVERSIDES (ATHERINOPSIDAE)

Freshwater habitats make up only ～0.01% of available aquatic habitat and yet harbor 40% of all fish species, whereas marine habitats comprise >99% of available aquatic habitat and have only 60% of fish species. One possible explanation for this pattern is that diversification rates are higher in freshwater habitats than in marine habitats. We investigated diversification in marine and freshwater lineages in the New World silverside fish clade Menidiinae (Teleostei, Atherinopsidae). Using a time‐calibrated phylogeny and a state‐dependent speciation–extinction framework, we determined the frequency and timing of habitat transitions in Menidiinae and tested for differences in diversification parameters between marine and freshwater lineages. We found that Menidiinae is an ancestrally marine lineage that independently colonized freshwater habitats four times followed by three reversals to the marine environment. Our state‐dependent diversification analyses showed that freshwater lineages have higher speciation and extinction rates than marine lineages. Net diversification rates were higher (but not significant) in freshwater than marine environments. The marine lineage‐through time (LTT) plot shows constant accumulation, suggesting that ecological limits to clade growth have not slowed diversification in marine lineages. Freshwater lineages exhibited an upturn near the recent in their LTT plot, which is consistent with our estimates of high background extinction rates. All sequence data are currently being archived on Genbank and phylogenetic trees archived on Treebase.