Adaptive radiation and the evolution of nectarivory in a large songbird clade

The accumulation of exceptional ecological diversity within a lineage is a key feature of adaptive radiation resulting from diversification associated with the subdivision of previously underutilized resources. The invasion of unoccupied niche space is predicted to be a key determinant of adaptive diversification, and this process may be particularly important if the diversity of competing lineages within the area, in which the radiation unfolds, is already high. Here, we test whether the evolution of nectarivory resulted in significantly higher rates of morphological evolution, more extensive morphological disparity, and a heightened build‐up of sympatric species diversity in a large adaptive radiation of passerine birds (the honeyeaters, about 190 species) that have diversified extensively throughout continental and insular settings. We find that a large increase in rates of body size evolution and general expansion in morphological space followed an ancestral shift to nectarivory, enabling the build‐up of large numbers of co‐occurring species that vary greatly in size, compared to related and co‐distributed nonnectarivorous clades. These results strongly support the idea that evolutionary shifts into novel areas of niche space play a key role in promoting adaptive radiation in the presence of likely competing lineages.     

Niche width impacts vertebrate diversification

Aim The size of the climatic niche of a species is a major factor determining its distribution and evolution. In particular, it has been proposed that niche width should be associated with the rate of species diversification. Here, we test whether species niche width affects the speciation and extinction rates of three main clades of vertebrates: amphibians, mammals and birds. Location Global. Methods We obtained the time‐calibrated phylogenies, IUCN conservation status, species distribution maps and climatic data for 2340 species of amphibians, 4563 species of mammals and 9823 species of birds. We computed the niche width for each species as the mean annual temperature across the species range. We estimated speciation, extinction and transition rates associated with lineages with either narrow (specialist) or wide (generalist) niches using phylogeny‐based birth–death models. We also tested if current conservation status was correlated with the niche width of species. Results We found higher net diversification rates in specialist species than in generalist species. This result was explained by both higher speciation rates (for the three taxonomic groups) and lower extinction rates (for mammals and birds only) in specialist than in generalist species. In contrast, current specialist species tended to be more threatened than generalist species. Main conclusions Our diversification analysis shows that the width of the climatic niche is strongly associated with diversification rates and may thus be a crucial factor for understanding the emergence of diversity patterns in vertebrates. The striking difference between our diversification results and current conservation status suggests that the current extinction process may be different from extinction rates estimated from the whole history of the group.     

Exploring the tempo of species diversification in legumes

Whatever criteria are used to measure evolutionary success – species numbers, geographic range, ecological abundance, ecological and life history diversity, background diversification rates, or the presence of rapidly evolving clades – the legume family is one of the most successful lineages of flowering plants. Despite this, we still know rather little about the dynamics of lineage and species diversification across the family through the Cenozoic, or about the underlying drivers of diversification. There have been few attempts to estimate net species diversification rates or underlying speciation and extinction rates for legume clades, to test whether among-lineage variation in diversification rates deviates from null expectations, or to locate species diversification rate shifts on specific branches of the legume phylogenetic tree. In this study, time-calibrated phylogenetic trees for a set of species-rich legume clades – Calliandra, Indigofereae, Lupinus, Mimosa and Robinieae – and for the legume family as a whole, are used to explore how we might approach these questions. These clades are analysed using recently developed maximum likelihood and Bayesian methods to detect species diversification rate shifts and test for among-lineage variation in speciation, extinction and net diversification rates. Possible explanations for rate shifts in terms of extrinsic factors and/or intrinsic trait evolution are discussed. In addition, several methodological issues and limitations associated with these analyses are highlighted emphasizing the potential to improve our understanding of the evolutionary dynamics of legume diversification by using much more densely sampled phylogenetic trees that integrate information across broad taxonomic, geographical and temporal levels.     

What explains patterns of species richness? The relative importance of climatic‐niche evolution,morphological evolution,and ecological limits in salamanders

A major goal of evolutionary biology and ecology is to understand why species richness varies among clades. Previous studies have suggested that variation in richness among clades might be related to variation in rates of morphological evolution among clades (e.g., body size and shape). Other studies have suggested that richness patterns might be related to variation in rates of climatic‐niche evolution. However, few studies, if any, have tested the relative importance of these variables in explaining patterns of richness among clades. Here, we test their relative importance among major clades of Plethodontidae, the most species‐rich family of salamanders. Earlier studies have suggested that climatic‐niche evolution explains patterns of diversification among plethodontid clades, whereas rates of morphological evolution do not. A subsequent study stated that rates of morphological evolution instead explained patterns of species richness among plethodontid clades (along with “ecological limits” on richness of clades, leading to saturation of clades with species, given limited resources). However, they did not consider climatic‐niche evolution. Using phylogenetic multiple regression, we show that rates of climatic‐niche evolution explain most variation in richness among plethodontid clades, whereas rates of morphological evolution do not. We find little evidence that ecological limits explain patterns of richness among plethodontid clades. We also test whether rates of morphological and climatic‐niche evolution are correlated, and find that they are not. Overall, our results help explain richness patterns in a major amphibian group and provide possibly the first test of the relative importance of climatic niches and morphological evolution in explaining diversity patterns.     

Habitat use affects morphological diversification in dragon lizards

Habitat use may lead to variation in diversity among evolutionary lineages because habitats differ in the variety of ways they allow for species to make a living. Here, we show that structural habitats contribute to differential diversification of limb and body form in dragon lizards (Agamidae). Based on phylogenetic analysis and ancestral state reconstructions for 90 species, we find that multiple lineages have independently adopted each of four habitat use types: rock‐dwelling, terrestriality, semi‐arboreality and arboreality. Given these reconstructions, we fit models of evolution to species’ morphological trait values and find that rock‐dwelling and arboreality limit diversification relative to terrestriality and semi‐arboreality. Models preferred by Akaike information criterion infer slower rates of size and shape evolution in lineages inferred to occupy rocks and trees, and model‐averaged rate estimates are slowest for these habitat types. These results suggest that ground‐dwelling facilitates ecomorphological differentiation and that use of trees or rocks impedes diversification.     

Larger brain size indirectly increases vulnerability to extinction in mammals

Although previous studies have addressed the question of why large brains evolved, we have limited understanding of potential beneficial or detrimental effects of enlarged brain size in the face of current threats. Using novel phylogenetic path analysis, we evaluated how brain size directly and indirectly, via its effects on life history and ecology, influences vulnerability to extinction across 474 mammalian species. We found that larger brains, controlling for body size, indirectly increase vulnerability to extinction by extending the gestation period, increasing weaning age, and limiting litter sizes. However, we found no evidence of direct, beneficial, or detrimental effects of brain size on vulnerability to extinction, even when we explicitly considered the different types of threats that lead to vulnerability. Order‐specific analyses revealed qualitatively similar patterns for Carnivora and Artiodactyla. Interestingly, for Primates, we found that larger brain size was directly (and indirectly) associated with increased vulnerability to extinction. Our results indicate that under current conditions, the constraints on life history imposed by large brains outweigh the potential benefits, undermining the resilience of the studied mammals. Contrary to the selective forces that have favored increased brain size throughout evolutionary history, at present, larger brains have become a burden for mammals.     

Diversity versus disparity and the radiation of modern cetaceans

Modern whales are frequently described as an adaptive radiation spurred by either the evolution of various key innovations (such as baleen or echolocation) or ecological opportunity following the demise of archaic whales. Recent analyses of diversification rate shifts on molecular phylogenies raise doubts about this interpretation since they find no evidence of increased speciation rates during the early evolution of modern taxa. However, one of the central predictions of ecological adaptive radiation is rapid phenotypic diversification, and the tempo of phenotypic evolution has yet to be quantified in cetaceans. Using a time-calibrated molecular phylogeny of extant cetaceans and a morphological dataset on size, we find evidence that cetacean lineages partitioned size niches early in the evolutionary history of neocetes and that changes in cetacean size are consistent with shifts in dietary strategy. We conclude that the signature of adaptive radiations may be retained within morphological traits even after equilibrium diversity has been reached and high extinction or fluctuations in net diversification have erased any signature of an early burst of diversification in the structure of the phylogeny.     

Shifts in Climate Foster Exceptional Opportunities for Species Radiation: The Case of South African Geraniums

Climate change is often assumed to be a major driver of biodiversity loss. However, it can also set the stage for novel diversification in lineages with the evolutionary ability to colonize new environments. Here we tested if the extraordinary evolutionary success of the genus Pelargonium was related to the ability of its species to capitalize on the climate niche variation produced by the historical changes in southern Africa. We evaluated the relationship between rates of climate niche evolution and diversification rates in the main Pelargonium lineages and disentangled the roles of deep and recent historical events in the modification of species niches. Pelargonium clades exhibiting higher ecological differentiation along summer precipitation (SPP) gradients also experienced higher diversification rates. Faster rates of niche differentiation in spatially structured variables, along with lower levels of niche overlap among closely related species, suggest recent modification in species niches (e.g. dispersal or range shift) and niche lability. We suggest that highly structured SPP gradients established during the aridification process within southern Africa, in concert with niche lability and low niche overlap, contributed to species divergence. These factors are likely to be responsible for the extensive diversification of other lineages in this diversity hot spot.     

Defensive spines are associated with large geographic range but not diversification in spiny ants (Hymenoptera: Formicidae: Polyrhachis)

Several prominent evolutionary theories propose mechanisms whereby the evolution of a defensive trait or suite of traits causes significant shifts in species diversification rate and niche evolution. We investigate the role of cuticular spines, a highly variable morphological defensive trait in the hyperdiverse ant genus Polyrhachis, on species diversification and geographic range size. Informed by key innovation theory and the escape-and-radiate hypothesis, we predicted that clades with longer spines would exhibit elevated rates of diversification and larger range sizes compared to clades with shorter spines. To address these predictions, we estimated phylogenetic relationships with a phylogenomic approach utilizing ultraconserved elements and compiled morphological and biogeographic trait databases. In contrast to the first prediction, we found no association between diversification rate and any trait (spine length, body size and range size), with the sole exception of a positive association between range size and diversification in one of three trait-based diversification analyses. However, we recovered a positive phylogenetic correlation between spine length and geographic range size, suggesting that spines promote expanded geographic range. Notably, these results were consistent across analyses using different phylogenetic inference approaches and spine trait measurement schemes. This study provides a rare investigation of the role of a defensive trait on geographic range size, and ultimately supports the hypothesis that defensive spines are a factor in increased range size in Polyrhachis ants. Furthermore, the lack of support for an association between spines and diversification, which contrasts with previous work demonstrating a positive association between spines and diversification rate, is intriguing and warrants further study.     

Geographic range size, life history and rates of diversification in Australian mammals

Abstract What causes species richness to vary among different groups of organisms? Two hypotheses are that large geographical ranges and fast life history either reduce extinction rates or raise speciation rates, elevating a clade's rate of diversification. Here we present a comparative analysis of these hypotheses using data on the phylogenetic relationships, geographical ranges and life history of the terrestrial mammal fauna of Australia. By comparing species richness patterns to null models, we show that species are distributed nonrandomly among genera. Using sister‐clade comparisons to control for clade age, we then find that faster diversification is significantly associated with larger geographical ranges and larger litters, but there is no evidence for an effect of body size or age at first breeding on diversification rates. We believe the most likely explanation for these patterns is that larger litters and geographical ranges increase diversification rates because they buffer species from extinction. We also discuss the possibility that positive effects of litter size and range size on diversification rates result from elevated speciation rates.     

Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae)

Habitat shifts are implicated as the cause of many vertebrate radiations, yet relatively few empirical studies quantify patterns of diversification following colonization of new habitats in fishes. The pufferfishes (family Tetraodon‐tidae) occur in several habitats, including coral reefs and freshwater, which are thought to provide ecological opportunity for adaptive radiation, and thus provide a unique system for testing the hypothesis that shifts to new habitats alter diversification rates. To test this hypothesis, we sequenced eight genes for 96 species of pufferfishes and closely related porcupine fishes, and added 19 species from sequences available in GenBank. We time‐calibrated the molecular phylogeny using three fossils, and performed several comparative analyses to test whether colonization of novel habitats led to shifts in the rate of speciation and body size evolution, central predictions of clades experiencing ecological adaptive radiation. Colonization of freshwater is associated with lower rates of cladogenesis in pufferfishes, although these lineages also exhibit accelerated rates of body size evolution. Increased rates of cladogenesis are associated with transitions to coral reefs, but reef lineages surprisingly exhibit significantly lower rates of body size evolution. These results suggest that ecological opportunity afforded by novel habitats may be limited for pufferfishes due to competition with other species, constraints relating to pufferfish life history and trophic ecology, and other factors.     

Early burst in body size evolution is uncoupled from species diversification in diving beetles (Dytiscidae)

Changes in morphology are often thought to be linked to changes in species diversification, which is expected to leave a signal of early burst (EB) in phenotypic traits. However, such signal is rarely recovered in empirical phylogenies, even for groups with well‐known adaptive radiation. Using a comprehensive phylogenetic approach in Dytiscidae, which harbours ~4,300 species with as much as 50‐fold variation in body size among them, we ask whether pattern of species diversification correlates with morphological evolution. Additionally, we test whether the large variation in body size is linked to habitat preference and whether the latter influences species turnover. We found, in sharp contrast to most animal groups, that Dytiscidae body size evolution follows an early‐burst model with subsequent high phylogenetic conservatism. However, we found no evidence for associated shifts in species diversification, which point to an uncoupled evolution of morphology and species diversification. We recovered the ancestral habitat of Dytiscidae as lentic (standing water), with many transitions to lotic habitat (running water) that are concomitant to a decrease in body size. Finally, we found no evidence for difference in net diversification rates between habitats nor difference in turnover in lentic and lotic species. This result, together with recent findings in dragonflies, contrasts with some theoretical expectations of the habitat stability hypothesis. Thus, a thorough reassessment of the impact of dispersal, gene flow and range size on the speciation process is needed to fully encompass the evolutionary consequences of the lentic–lotic divide for freshwater fauna.     

Niche evolution and diversification in a Neotropical radiation of birds (Aves: Furnariidae)

Rapid diversification may be caused by ecological adaptive radiation via niche divergence. In this model, speciation is coupled with niche divergence and lineage diversification is predicted to be correlated with rates of niche evolution. Studies of the role of niche evolution in diversification have generally focused on ecomorphological diversification but climatic‐niche evolution may also be important. We tested these alternatives using a phylogeny of 298 species of ovenbirds (Aves: Furnariidae). We found that within Furnariidae, variation in species richness and diversification rates of subclades were best predicted by rate of climatic‐niche evolution than ecomorphological evolution. Although both are clearly important, univariate regression and multivariate model averaging more consistently supported the climatic‐niche as the best predictor of lineage diversification. Our study adds to the growing body of evidence, suggesting that climatic‐niche divergence may be an important driver of rapid diversification in addition to ecomorphological evolution. However, this pattern may depend on the phylogenetic scale at which rate heterogeneity is examined.     

Evolutionary Divergence in Brain Size between Migratory and Resident Birds

Despite important recent progress in our understanding of brain evolution, controversy remains regarding the evolutionary forces that have driven its enormous diversification in size. Here, we report that in passerine birds, migratory species tend to have brains that are substantially smaller (relative to body size) than those of resident species, confirming and generalizing previous studies. Phylogenetic reconstructions based on Bayesian Markov chain methods suggest an evolutionary scenario in which some large brained tropical passerines that invaded more seasonal regions evolved migratory behavior and migration itself selected for smaller brain size. Selection for smaller brains in migratory birds may arise from the energetic and developmental costs associated with a highly mobile life cycle, a possibility that is supported by a path analysis. Nevertheless, an important fraction (over 68%) of the correlation between brain mass and migratory distance comes from a direct effect of migration on brain size, perhaps reflecting costs associated with cognitive functions that have become less necessary in migratory species. Overall, our results highlight the importance of retrospective analyses in identifying selective pressures that have shaped brain evolution, and indicate that when it comes to the brain, larger is not always better.     

Repeated evolution and reversibility of self‐fertilization in the volvocine green algae*

Outcrossing and self‐fertilization are fundamental strategies of sexual reproduction, each with different evolutionary costs and benefits. Self‐fertilization is thought to be an evolutionary “dead‐end” strategy, beneficial in the short term but costly in the long term, resulting in self‐fertilizing species that occupy only the tips of phylogenetic trees. Here, we use volvocine green algae to investigate the evolution of self‐fertilization. We use ancestral‐state reconstructions to show that self‐fertilization has repeatedly evolved from outcrossing ancestors and that multiple reversals from selfing to outcrossing have occurred. We use three phylogenetic metrics to show that self‐fertilization is not restricted to the tips of the phylogenetic tree, a finding inconsistent with the view of self‐fertilization as a dead‐end strategy. We also find no evidence for higher extinction rates or lower speciation rates in selfing lineages. We find that self‐fertilizing species have significantly larger colonies than outcrossing species, suggesting the benefits of selfing may counteract the costs of increased size. We speculate that our macroevolutionary results on self‐fertilization (i.e., non‐tippy distribution, no decreased diversification rates) may be explained by the haploid‐dominant life cycle that occurs in volvocine algae, which may alter the costs and benefits of selfing.     

Symbiosis catalyses niche expansion and diversification

Interactions between species are important catalysts of the evolutionary processes that generate the remarkable diversity of life. Symbioses, conspicuous and inherently interesting forms of species interaction, are pervasive throughout the tree of life. However, nearly all studies of the impact of species interactions on diversification have concentrated on competition and predation leaving unclear the importance of symbiotic interaction. Here, I show that, as predicted by evolutionary theories of symbiosis and diversification, multiple origins of a key innovation, symbiosis between gall-inducing insects and fungi, catalysed both expansion in resource use (niche expansion) and diversification. Symbiotic lineages have undergone a more than sevenfold expansion in the range of host-plant taxa they use relative to lineages without such fungal symbionts, as defined by the genetic distance between host plants. Furthermore, symbiotic gall-inducing insects are more than 17 times as diverse as their non-symbiotic relatives. These results demonstrate that the evolution of symbiotic interaction leads to niche expansion, which in turn catalyses diversification.     

Key innovations and island colonization as engines of evolutionary diversification: a comparative test with the Australasian diplodactyloid geckos

The acquisition of key innovations and the invasion of new areas constitute two major processes that facilitate ecological opportunity and subsequent evolutionary diversification. Using a major lizard radiation as a model, the Australasian diplodactyloid geckos, we explored the effects of two key innovations (adhesive toepads and a snake‐like phenotype) and the invasion of new environments (island colonization) in promoting the evolution of phenotypic and species diversity. We found no evidence that toepads had significantly increased evolutionary diversification, which challenges the common assumption that the evolution of toepads has been responsible for the extensive radiation of geckos. In contrast, a snakelike phenotype was associated with increased rates of body size evolution and, to a lesser extent, species diversification. However, the clearest impact on evolutionary diversification has been the colonization of New Zealand and New Caledonia, which were associated with increased rates of both body size evolution and species diversification. This highlights that colonizing new environments can drive adaptive diversification in conjunction or independently of the evolution of a key innovation. Studies wishing to confirm the putative link between a key innovation and subsequent evolutionary diversification must therefore show that it has been the acquisition of an innovation specifically, not the colonization of new areas more generally, that has prompted diversification.     

Evolution and ecology of lizard body sizes

Aim Body size is instrumental in influencing animal physiology, morphology, ecology and evolution, as well as extinction risk. I examine several hypotheses regarding the influence of body size on lizard evolution and extinction risk, assessing whether body size influences, or is influenced by, species richness, herbivory, island dwelling and extinction risk. Location World‐wide. Methods I used literature data and measurements of museum and live specimens to estimate lizard body size distributions. Results I obtained body size data for 99% of the world's lizard species. The body size–frequency distribution is highly modal and right skewed and similar distributions characterize most lizard families and lizard assemblages across biogeographical realms. There is a strong negative correlation between mean body size within families and species richness. Herbivorous lizards are larger than omnivorous and carnivorous ones, and aquatic lizards are larger than non‐aquatic species. Diurnal activity is associated with small body size. Insular lizards tend towards both extremes of the size spectrum. Extinction risk increases with body size of species for which risk has been assessed. Main conclusions Small size seems to promote fast diversification of disparate body plans. The absence of mammalian predators allows insular lizards to attain larger body sizes by means of release from predation and allows them to evolve into the top predator niche. Island living also promotes a high frequency of herbivory, which is also associated with large size. Aquatic and nocturnal lizards probably evolve large size because of thermal constraints. The association between large size and high extinction risk, however, probably reflects a bias in the species in which risk has been studied.     

The importance (or lack thereof) of niche divergence to the maintenance of a northern species complex: the case of the long‐toed salamander (Ambystoma macrodactylum Baird)

The relative importance of ecological vs. nonecological factors for the origin and maintenance of species is an open question in evolutionary biology. Young lineages – such as the distinct genetic groups that make up the ranges of many northern species – represent an opportunity to study the importance of ecological divergence during the early stages of diversification. Yet, few studies have examined the extent of niche divergence between lineages in previously glaciated regions and the role of ecology in maintaining the contact zones between them. In this study, we used tests of niche overlap in combination with ecological niche models to explore the extent of niche divergence between lineages of the long‐toed salamander (Ambystoma macrodactylum Baird) species complex and to determine whether contact zones correspond to (divergent) niche limits. We found limited evidence for niche divergence between the different long‐toed salamander lineages, substantial overlap in the predicted distribution of suitable climatic space for all lineages and range limits that are independent of niche limits. These results raise questions as to the importance of ecological divergence to the development of this widespread species complex and highlight the potential for non‐ecological factors to play a more important role in the maintenance of northern taxa.     

Evolution of brain region volumes during artificial selection for relative brain size

The vertebrate brain shows an extremely conserved layout across taxa. Still, the relative sizes of separate brain regions vary markedly between species. One interesting pattern is that larger brains seem associated with increased relative sizes only of certain brain regions, for instance telencephalon and cerebellum. Till now, the evolutionary association between separate brain regions and overall brain size is based on comparative evidence and remains experimentally untested. Here, we test the evolutionary response of brain regions to directional selection on brain size in guppies (Poecilia reticulata) selected for large and small relative brain size. In these animals, artificial selection led to a fast response in relative brain size, while body size remained unchanged. We use microcomputer tomography to investigate how the volumes of 11 main brain regions respond to selection for larger versus smaller brains. We found no differences in relative brain region volumes between large‐ and small‐brained animals and only minor sex‐specific variation. Also, selection did not change allometric scaling between brain and brain region sizes. Our results suggest that brain regions respond similarly to strong directional selection on relative brain size, which indicates that brain anatomy variation in contemporary species most likely stem from direct selection on key regions.