Detecting the historical signature of key innovations using stochastic models of character evolution and cladogenesis

Phylogenetic evidence for biological traits that increase the net diversification rate of lineages (key innovations) is most commonly drawn from comparisons of clade size. This can work well for ancient, unreversed traits and for correlating multiple trait origins with higher diversification rates, but it is less suitable for unique events, recently evolved innovations, and traits that exhibit homoplasy. Here I present a new method for detecting the phylogenetic signature of key innovations that tests whether the evolutionary history of the candidate trait is associated with shorter waiting times between cladogenesis events. The method employs stochastic models of character evolution and cladogenesis and integrates well into a Bayesian framework in which uncertainty in historical inferences (such as phylogenetic relationships) is allowed. Applied to a well-known example in plants, nectar spurs in columbines, the method gives much stronger support to the key innovation hypothesis than previous tests.     

Digging their own macroevolutionary grave: fossoriality as an evolutionary dead end in snakes

The tree of life is highly asymmetrical in its clade wise species richness, and this has often been attributed to variation in diversification rates either across time or lineages. Variations across lineages are usually associated with traits that increase lineage diversification. Certain traits can also hinder diversification by increasing extinction, and such traits are called evolutionary dead ends. Ecological specialization has usually been considered as an evolutionary dead end. However, recent analyses of specializations along single axes have provided mixed support for this model. Here, we test if fossoriality, a trait that forces specialization at multiple axes, acts as an evolutionary dead end in squamates (lizards and snakes) using recently developed phylogenetic comparative methods. We show that fossoriality is an evolutionary dead end in snakes but not in lizards. Fossorial snakes exhibit reduced speciation and increased extinction compared to nonfossorial snakes. Our analysis also indicates that transition rates from fossoriality to nonfossoriality in snakes are significantly lower than transition rates from nonfossoriality to fossoriality. Overall our results suggest that broad‐scale ecological interactions that lead to specialization at multiple axes limit diversification.     

A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts

When novel sources of ecological opportunity are available, physiological innovations can trigger adaptive radiations. This could be the case of yeasts (Saccharomycotina), in which an evolutionary novelty is represented by the capacity to exploit simple sugars from fruits (fermentation). During adaptive radiations, diversification and morphological evolution are predicted to slow‐down after early bursts of diversification. Here, we performed the first comparative phylogenetic analysis in yeasts, testing the “early burst” prediction on species diversification and also on traits of putative ecological relevance (cell‐size and fermentation versatility). We found that speciation rates are constant during the time‐range we considered (ca., 150 millions of years). Phylogenetic signal of both traits was significant (but lower for cell‐size), suggesting that lineages resemble each other in trait‐values. Disparity analysis suggested accelerated evolution (diversification in trait values above Brownian Motion expectations) in cell‐size. We also found a significant phylogenetic regression between cell‐size and fermentation versatility (R² = 0.10), which suggests correlated evolution between both traits. Overall, our results do not support the early burst prediction both in species and traits, but suggest a number of interesting evolutionary patterns, that warrant further exploration. For instance, we show that the Whole Genomic Duplication that affected a whole clade of yeasts, does not seems to have a statistically detectable phenotypic effect at our level of analysis. In this regard, further studies of fermentation under common‐garden conditions combined with comparative analyses are warranted.     

Defensive traits exhibit an evolutionary trade‐off and drive diversification in ants

Evolutionary biologists have long predicted that evolutionary trade‐offs among traits should constrain morphological divergence and species diversification. However, this prediction has yet to be tested in a broad evolutionary context in many diverse clades, including ants. Here, we reconstruct an expanded ant phylogeny representing 82% of ant genera, compile a new family‐wide trait database, and conduct various trait‐based analyses to show that defensive traits in ants do exhibit an evolutionary trade‐off. In particular, the use of a functional sting negatively correlates with a suite of other defensive traits including spines, large eye size, and large colony size. Furthermore, we find that several of the defensive traits that trade off with a sting are also positively correlated with each other and drive increased diversification, further suggesting that these traits form a defensive suite. Our results support the hypothesis that trade‐offs in defensive traits significantly constrain trait evolution and influence species diversification in ants.     

Spatial processes and evolutionary models: a critical review

Evolution is a fundamentally population level process in which variation, drift and selection produce both temporal and spatial patterns of change. Statistical model fitting is now commonly used to estimate which kind of evolutionary process best explains patterns of change through time using models like Brownian motion, stabilizing selection (Ornstein–Uhlenbeck) and directional selection on traits measured from stratigraphic sequences or on phylogenetic trees. But these models assume that the traits possessed by a species are homogeneous. Spatial processes such as dispersal, gene flow and geographical range changes can produce patterns of trait evolution that do not fit the expectations of standard models, even when evolution at the local‐population level is governed by drift or a typical OU model of selection. The basic properties of population level processes (variation, drift, selection and population size) are reviewed and the relationship between their spatial and temporal dynamics is discussed. Typical evolutionary models used in palaeontology incorporate the temporal component of these dynamics, but not the spatial. Range expansions and contractions introduce rate variability into drift processes, range expansion under a drift model can drive directional change in trait evolution, and spatial selection gradients can create spatial variation in traits that can produce long‐term directional trends and punctuation events depending on the balance between selection strength, gene flow, extirpation probability and model of speciation. Using computational modelling that spatial processes can create evolutionary outcomes that depart from basic population‐level notions from these standard macroevolutionary models.     

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.     

Trait-dependent diversification and the impact of palaeontological data on evolutionary hypothesis testing in New World ratsnakes (tribe Lampropeltini)

For studies investigating trait evolution, there are at least two important questions. First, have traits under consideration influenced cladogenesis and extinction in the group? Second, how do fossil data alter inferences about trait evolution or diversification‐rate dynamics? However, relatively few studies have assessed these questions. Here, we use recently developed methods to test for trait‐dependent diversification in the New World colubrid snake tribe Lampropeltini. We also integrate data from fossil taxa into phylogenetic estimation of evolutionary parameters using a simple Monte Carlo randomization test. These analyses suggest that ecological conditions in temperate regions are tied to higher rates of cladogenesis, but that body size is not related to diversification in the group. We also find that the inclusion of fossil taxa alters absolute estimates of size and the rate of size evolution, but not the overall pattern of ecomorphological diversification, as well as estimates of evolutionary rates, particularly extinction.     

Cope's rule and the adaptive landscape of dinosaur body size evolution

The largest known dinosaurs weighed at least 20 million times as much as the smallest, indicating exceptional phenotypic divergence. Previous studies have focused on extreme giant sizes, tests of Cope's rule, and miniaturization on the line leading to birds. We use non‐uniform macroevolutionary models based on Ornstein–Uhlenbeck and trend processes to unify these observations, asking: what patterns of evolutionary rates, directionality and constraint explain the diversification of dinosaur body mass? We find that dinosaur evolution is constrained by attraction to discrete body size optima that undergo rare, but abrupt, evolutionary shifts. This model explains both the rarity of multi‐lineage directional trends, and the occurrence of abrupt directional excursions during the origins of groups such as tiny pygostylian birds and giant sauropods. Most expansion of trait space results from rare, constraint‐breaking innovations in just a small number of lineages. These lineages shifted rapidly into novel regions of trait space, occasionally to small sizes, but most often to large or giant sizes. As with Cenozoic mammals, intermediate body sizes were typically attained only transiently by lineages on a trajectory from small to large size. This demonstrates that bimodality in the macroevolutionary adaptive landscape for land vertebrates has existed for more than 200 million years.     

Terrestrialization, miniaturization and rates of diversification in African puddle frogs (Anura: Phrynobatrachidae)

Terrestrialization, the evolution of non-aquatic oviposition, and miniaturization, the evolution of tiny adult body size, are recurring trends in amphibian evolution, but the relationships among the traits that characterize these phenomena are not well understood. Furthermore, these traits have been identified as possible "key innovations" that are predicted to increase rates of speciation in those lineages in which they evolve. We examine terrestrialization and miniaturization in sub-Saharan puddle frogs (Phrynobatrachidae) in a phylogenetic context to investigate the relationship between adaptation and diversification through time. We use relative dating techniques to ascertain if character trait shifts are associated with increased diversification rates, and we evaluate the likelihood that a single temporal event can explain the evolution of those traits. Results indicate alternate reproductive modes evolved independently in Phrynobatrachus at least seven times, including terrestrial deposition of eggs and terrestrial, non-feeding larvae. These shifts towards alternate reproductive modes are not linked to a common temporal event. Contrary to the "key innovations" hypothesis, clades that exhibit alternate reproductive modes have lower diversification rates than those that deposit eggs aquatically. Adult habitat, pedal webbing and body size have no effect on diversification rates. Though these traits putatively identified as key innovations for Phrynobatrachus do not seem to be associated with increased speciation rates, they may still provide opportunities to extend into new niches, thus increasing overall diversity.     

One size fits all? Determinants of sperm transfer in a highly dimorphic orb‐web spider

The evolutionary significance of widespread hypo‐allometric scaling of genital traits in combination with rapid interspecific genital trait divergence has been of key interest to evolutionary biologists for many years and remains poorly understood. Here, we provide a detailed assessment of quantitative genital trait variation in males and females of the sexually highly dimorphic and cannibalistic orb‐weaving spider Argiope aurantia. We then test how this trait variation relates to sperm transfer success. In particular, we test specific predictions of the one‐size‐fits‐all and lock‐and‐key hypotheses for the evolution of genital characters. We use video‐taped staged matings in a controlled environment with subsequent morphological microdissections and sperm count analyses. We find little support for the prediction of the one‐size‐fits‐all hypothesis for the evolution of hypo‐allometric scaling of genital traits, namely that intermediate trait dimensions confer highest sperm transfer success. Likewise, our findings do not support the prediction of the lock‐and‐key hypothesis that a tight fit of male and female genital traits mediates highest sperm transfer success. We do, however, detect directional effects of a number of male and female genital characters on sperm transfer, suggesting that genital trait dimensions are commonly under selection in nature. Importantly, even though females are much larger than males, spermatheca size limits the number of sperm transferred, contradicting a previous hypothesis about the evolutionary consequences of genital size dimorphism in extremely size‐dimorphic taxa. We also find strong positive effects of male body size and copulation duration on the probability of sperm transfer and the number of sperm transferred, with implications for the evolution of extreme sexual size dimorphism and sexual cannibalism in orb weavers.     

Eating down the food chain: generalism is not an evolutionary dead end for herbivores

The role of trophic specialisation in taxonomic diversification remains unclear. Plant specialists diversify faster than omnivores and animalivores, but at shorter macroevolutionary scales this pattern sometimes reverses. Here, we estimate the effect of diet diversification on speciation rates in noctilionoid bats, controlling for tree shape, rate heterogeneity and macroevolutionary regimes. We hypothesise that niche subdivision among herbivores positively relates to speciation rates, differing between macroevolutionary regimes. We found the rate at which new herbivorous lineages originate decreases as rates of diet evolution increase. Herbivores experience higher speciation rates, but generalist herbivores and predominantly herbivorous omnivores speciate faster than specialised herbivores, omnivores and animalivores. Generalised herbivory is not a dead end. We show that analysing ecological traits and diversification requires accounting for macroevolutionary regimes and within‐ and between‐clade variation in evolutionary rates. Our approach overcomes the high false‐positive rates of other methods and illuminates the roles of herbivory and specialisation in speciation.     

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.     

Parallel adaptations to nectarivory in parrots,key innovations and the diversification of the Loriinae

Specialization to nectarivory is associated with radiations within different bird groups, including parrots. One of them, the Australasian lories, were shown to be unexpectedly species rich. Their shift to nectarivory may have created an ecological opportunity promoting species proliferation. Several morphological specializations of the feeding tract to nectarivory have been described for parrots. However, they have never been assessed in a quantitative framework considering phylogenetic nonindependence. Using a phylogenetic comparative approach with broad taxon sampling and 15 continuous characters of the digestive tract, we demonstrate that nectarivorous parrots differ in several traits from the remaining parrots. These trait‐changes indicate phenotype–environment correlations and parallel evolution, and may reflect adaptations to feed effectively on nectar. Moreover, the diet shift was associated with significant trait shifts at the base of the radiation of the lories, as shown by an alternative statistical approach. Their diet shift might be considered as an evolutionary key innovation which promoted significant non‐adaptive lineage diversification through allopatric partitioning of the same new niche. The lack of increased rates of cladogenesis in other nectarivorous parrots indicates that evolutionary innovations need not be associated one‐to‐one with diversification events.     

Genomic and phenomic analysis of island ant community assembly

Island biodiversity has long fascinated biologists as it typically presents tractable systems for unpicking the eco‐evolutionary processes driving community assembly. In general, two recurring themes are of central theoretical interest. First, immigration, diversification, and extinction typically depend on island geographical properties (e.g., area, isolation, and age). Second, predictable ecological and evolutionary trajectories readily occur after colonization, such as the evolution of adaptive trait syndromes, trends toward specialization, adaptive radiation, and eventual ecological decline. Hypotheses such as the taxon cycle draw on several of these themes to posit particular constraints on colonization and subsequent eco‐evolutionary dynamics. However, it has been challenging to examine these integrated dynamics with traditional methods. Here, we combine phylogenomics, population genomics and phenomics, to unravel community assembly dynamics among Pheidole (Hymenoptera, Formicidae) ants in the isolated Fijian archipelago. We uphold basic island biogeographic predictions that isolated islands accumulate diversity primarily through in situ evolution rather than dispersal, and population genomic support for taxon cycle predictions that endemic species have decreased dispersal ability and demography relative to regionally widespread taxa. However, rather than trending toward island syndromes, ecomorphological diversification in Fiji was intense, filling much of the genus‐level global morphospace. Furthermore, while most endemic species exhibit demographic decline and reduced dispersal, we show that the archipelago is not an evolutionary dead‐end. Rather, several endemic species show signatures of population and range expansion, including a successful colonization to the Cook islands. These results shed light on the processes shaping island biotas and refine our understanding of island biogeographic theory.     

Is specialization an evolutionary dead end? Testing for differences in speciation,extinction and trait transition rates across diverse phylogenies of specialists and generalists

Specialization has often been claimed to be an evolutionary dead end, with specialist lineages having a reduced capacity to persist or diversify. In a phylogenetic comparative framework, an evolutionary dead end may be detectable from the phylogenetic distribution of specialists, if specialists rarely give rise to large, diverse clades. Previous phylogenetic studies of the influence of specialization on macroevolutionary processes have demonstrated a range of patterns, including examples where specialists have both higher and lower diversification rates than generalists, as well as examples where the rates of evolutionary transitions from generalists to specialists are higher, lower or equal to transitions from specialists to generalists. Here, we wish to ask whether these varied answers are due to the differences in macroevolutionary processes in different clades, or partly due to differences in methodology. We analysed ten phylogenies containing multiple independent origins of specialization and quantified the phylogenetic distribution of specialists by applying a common set of metrics to all datasets. We compared the tip branch lengths of specialists to generalists, the size of specialist clades arising from each evolutionary origin of a specialized trait and whether specialists tend to be clustered or scattered on phylogenies. For each of these measures, we compared the observed values to expectations under null models of trait evolution and expected outcomes under alternative macroevolutionary scenarios. We found that specialization is sometimes an evolutionary dead end: in two of the ten case studies (pollinator‐specific plants and host‐specific flies), specialization is associated with a reduced rate of diversification or trait persistence. However, in the majority of studies, we could not distinguish the observed phylogenetic distribution of specialists from null models in which specialization has no effect on diversification or trait persistence.     

MORPHOLOGICAL RATES OF ANGIOSPERM SEED SIZE EVOLUTION

The evolution of seed size among angiosperms reflects their ecological diversification in a complex fitness landscape of life‐history strategies. The lineages that have evolved seeds beyond the upper and lower boundaries that defined nonflowering seed plants since the Paleozoic are more dispersed across the angiosperm phylogeny than would be expected under a neutral model of phenotypic evolution. Morphological rates of seed size evolution estimated for 40 clades based on 17,375 species ranged from 0.001 (Garryales) to 0.207 (Malvales). Comparative phylogenetic analysis indicated that morphological rates are not associated with the clade's seed size but are negatively correlated with the clade's position in the overall distribution of angiosperm seed sizes; clades with seed sizes closer to the angiosperm mean had significantly higher morphological rates than clades with extremely small or extremely large seeds. Likewise, per‐clade taxonomic diversification rates are not associated with the seed size of the clade but with where the clade falls within the angiosperm seed size distribution. These results suggest that evolutionary rates (morphological and taxonomic) are elevated in densely occupied regions of the seed morphospace relative to lineages whose ecophenotypic innovations have moved them toward the edges.     

Associated evolution of fruit size,fruit colour and spines in Neotropical palms

Understanding how ecological interactions have shaped the evolutionary dynamics of species traits remains a challenge in evolutionary ecology. Combining trait evolution models and phylogenies, we analysed the evolution of characters associated with seed dispersal (fruit size and colour) and herbivory (spines) in Neotropical palms to infer the role of these opposing animal–plant interactions in driving evolutionary patterns. We found that the evolution of fruit colour and fruit size was associated in Neotropical palms, supporting the adaptive interpretation of seed‐dispersal syndromes and highlighting the role of frugivores in shaping plant evolution. Furthermore, we revealed a positive association between fruit size and the presence of spines on palm leaves, bracteas and stems. We hypothesize that interactions between palms and large‐bodied frugivores/herbivores may explain the evolutionary relationship between fruit size and spines. Large‐bodied frugivores, such as extinct megafauna, besides consuming the fruits and dispersing large seeds, may also have consumed the leaves or damaged the plants, thus simultaneously favouring the evolution of large fruits and defensive structures. Our findings show how current trait patterns can be understood as the result of the interplay between antagonistic and mutualistic interactions that have happened throughout the evolutionary history of a clade.     

Are spurred cyathia a key innovation? Molecular systematics and trait evolution in the slipper spurges (Pedilanthus clade: Euphorbia, Euphorbiaceae)

The study of traits that play a key role in promoting diversification is central to evolutionary biology. Floral nectar spurs are among the few plant traits that correlate with an enhanced rate of diversification, supporting the claim that they are key innovations. Slight changes in spur morphology could confer some degree of premating isolation, explaining why clades with spurs tend to include more species than their spurless close relatives. We explored whether the cyathial nectar spur of the Pedilanthus clade (Euphorbia) may also function as a key innovation. We estimated the phylogeny of the Pedilanthus clade using one plastid (matK) and three nuclear regions (ITS and two G3pdh loci) and used our results and a Yule model of diversification to test the hypothesis that the cyathial spur correlates with an increased diversification rate. We found a lack of statistical support for the key innovation hypothesis unless specific assumptions regarding the phylogeny apply. However, the young age (hence small size) of the group may limit our ability to detect a significant increase in diversification rate. Additionally, our results confirm previous species designations, indicate higher homoplasy in cyathial than in vegetative features, and suggest a possible Central American origin of the group.     

Differential Evolution of Advertisement Call Traits in Dart-Poison Frogs (Anura: Dendrobatidae)

The ability to recognise and discriminate between heterospecific and conspecific individuals plays an essential role in mate choice, reproductive isolation and thus species diversification. Many animals discriminate based on advertisement calls, whose evolution may be driven by a variety of forces such as natural selection, sexual selection or stochastic processes. The relative importance of stochastic processes acting on a given trait is usually correlated with its phylogenetic signal. Mate-recognition signals are complex traits composed of multiple features that could potentially respond independently to evolutionary forces. The advertisement call of anurans is used in species recognition and mate choice. In this study, we estimate the phylogenetic signal for body size and a suite of traits describing the male advertisement call from dart-poison frogs (Anura: Dendrobatidae). We found a surprisingly high phylogenetic signal for all call traits. In addition, call traits varied in their degree of phylogenetic signal, suggesting that evolutionary forces have been acting differently on different traits. Pulse duration showed the strongest phylogenetic signal. Peak frequency and body size were correlated and presented high phylogenetic signal indicating that the evolution of one trait may be driving or constraining the other. Since most variation in call traits can be explained by the phylogenetic history of the species, we cannot reject the hypothesis that stochastic processes account for significant evolutionary divergence in frog calls.