PHYLOGENETIC ANALYSIS OF TRAIT EVOLUTION AND SPECIES DIVERSITY VARIATION AMONG ANGIOSPERM FAMILIES

Angiosperm families differ greatly from one another in species richness (S). Previous studies have attributed significant components of this variation to the influence of pollination mode (biotic/abiotic) and growth form (herbaceous/woody) on speciation rate, but these results suffer difficulties of interpretation because all the studies ignored the phylogenetic relationships among families. We use a molecular phylogeny of the angiosperm families to reanalyse correlations between S and family-level traits and use reconstructions of trait evolution to interpret the results. We confirm that pollination mode and growth form are correlated with S and show that the majority of changes in pollination mode involved a change from biotic to abiotic pollination with an associated fall in speciation rate. The majority of growth form changes involved the evolution of herbaceousness from woodiness with a correlated rise in speciation rate. We test the hypothesis of Ricklefs and Renner (1994) that “evolutionary flexibility” rather than other trait changes triggered increased speciation rates in some families, but find little support for the hypothesis.     

Correlated divergence of female and male genitalia in replicated lineages with ongoing ecological speciation

Divergence of genital traits among lineages has the potential to serve as a reproductive isolating barrier when copulation, insemination, and fertilization are inhibited by incompatibilities between female and male genitalia. Despite widespread evidence for genital trait diversity among closely related lineages and coevolution of female and male genitalia within lineages, few studies have investigated genital evolution during the early stages of speciation. We quantified genital variation in replicated population pairs of Poecilia mexicana with ongoing ecological speciation between sulfidic (H₂S containing) and nearby nonsulfidic habitats. These analyses revealed rapid and correlated divergence of female and male genitalia across evolutionarily independent population pairs exposed to divergent selection regimes. Both sexes exhibited convergent evolution of genital traits among populations inhabiting similar habitat types. Our results demonstrate that genital evolution can occur during the early stages of speciation‐with‐gene‐flow, potentially as a result of variation in the intensity of sexual conflict among populations. Our results suggest genitalia may contribute to early stages of divergence and challenge the generality of previously suggested mechanisms of genital evolution in poeciliids.     

Patterns and processes in the evolutionary history of parrotfishes (Family Labridae)

Phylogenetic reconstruction of the evolutionary relationships among 61 of the 70 species of the parrotfish genera Chlorurus and Scarus (Family Labridae) based on mitochondrial and nuclear gene sequences retrieved 15 well‐supported clades with mid Pliocene/Pleistocene diversification. Twenty‐two reciprocally monophyletic sister‐species pairs were identified: 64% were allopatric, and the remainder were sympatric. Age of divergence was similar for allopatric and sympatric species pairs. Sympatric sister pairs displayed greater divergence in morphology, ecology, and sexually dimorphic colour patterns than did allopatric pairs, suggesting that both genetic drift in allopatric species pairs and ecologically adaptive divergence between members of sympatric pairs have played a role in diversification. Basal species typically have small geographical ranges and are restricted to geographically and ecologically peripheral reef habitats. We found little evidence that a single dominant process has driven diversification, nor did we detect a pattern of discrete, sequential stages of diversification in relation to habitat, ecology, and reproductive biology. The evolution of Chlorurus and Scarus has been complex, involving a number of speciation processes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 529–557.     

Evolution and plasticity: Divergence of song discrimination is faster in birds with innate song than in song learners in Neotropical passerine birds

Plasticity is often thought to accelerate trait evolution and speciation. For example, plasticity in birdsong may partially explain why clades of song learners are more diverse than related clades with innate song. This “song learning” hypothesis predicts that (1) differences in song traits evolve faster in song learners, and (2) behavioral discrimination against allopatric song (a proxy for premating reproductive isolation) evolves faster in song learners. We tested these predictions by analyzing acoustic traits and conducting playback experiments in allopatric Central American sister pairs of song learning oscines (N = 42) and nonlearning suboscines (N = 27). We found that nonlearners evolved mean acoustic differences slightly faster than did leaners, and that the mean evolutionary rate of song discrimination was 4.3 times faster in nonlearners than in learners. These unexpected results may be a consequence of significantly greater variability in song traits in song learners (by 54–79%) that requires song‐learning oscines to evolve greater absolute differences in song before achieving the same level of behavioral song discrimination as nonlearning suboscines. This points to “a downside of learning” for the evolution of species discrimination, and represents an important example of plasticity reducing the rate of evolution and diversification by increasing variability.     

Covariation among floral traits in Spergularia marina (Caryophyllaceae): geographic and temporal variation in phenotypic and among-family correlations

Strong covariation among traits suggests the presence of constraints on their independent evolution due to pleiotropy, to linkage, or to selective forces that maintain particular trait combinations. We examined floral trait covariation among individuals, among maternal families within and across populations, and over time, in greenhouse-raised plants of the autogamous Spergularia marina. We had three aims. First, since the phenotype of traits expressed by modular organs often changes as individuals age, estimates of the degree of genetic covariation between such traits may also change over time. To seek evidence for this, we measured weekly (for five weeks) an array of floral traits among plants representing ～ 10 maternal families from each of four populations. The statistical significance of the phenotypic and among-family correlations among traits changed over time. Second, we compared populations with respect to trait covariation to determine whether populations or traits appear to be evolving independently of one another. Differences observed among populations suggest that they have diverged genetically. Third, we sought correlations that might reflect constraints on the independent evolution of floral traits. Investment in another and ovule production per flower vary independently among maternal families; there was no evidence for a “trade-off” between male and female investment. We propose that in autogamous taxa one should not find a negative correlation between pollen and ovule production per flower, as such taxa cannot evolve sexual specialization and should be under strong selection to maintain an efficient pollen:ovule ratio, preventing the evolution of male-biased or female-biased genotypes. We found that other pairs of floral traits, however, expressed highly signficant correlation coefficients, suggesting the presence of some evolutionary constraints, at least within some populations, although their strength depended on exactly when flowers were sampled.     

The evolutionary potential of developmental instability

Whether or not developmental instability (DI) has evolutionary potential is subject to much debate. Generally, studies fail to detect significant heritability for fluctuating asymmetry (FA), a trait assumed to reflect DI. In addition, between‐trait correlations in FA are low, suggesting that DI is trait‐ rather than individual‐specific. Among the various attempts to explain these patterns, the overall weak correlation between FA and DI at the individual level has received most attention. Presently, the concept of hypothetical repeatability (R) of individual FA allows us to correct for this weak relationship, transforming patterns of FA into unbiased patterns of DI. By applying R to data presented in the literature, we show that heritability of DI remains lower than predicted but between‐trait correlations in DI substantially increase after transformation. We further provide evidence that DI changes from a trait‐ to an individual‐specific property with higher values of R. As increasing hypothetical repeatability might co‐occur with increased environmental or genetic stress, we discuss the potential implications of our results for the study of evolution of stress resistance. From this we conclude that there is an urgent need for studies that compare the evolutionary potential of developmental instability under a variety of stress conditions.     

An assessment of Putative Sexually Antagonistic Traits in a Freshwater Amphipod Species

Sexual conflict can result in an ‘evolutionary arms race’ between males and females, with the evolution of sexual antagonistic traits used to resolve the conflict in favor of one sex over the other. We assessed the resolution of sexual conflict in a Hyalella amphipod species by manipulating putative sexually antagonistic traits in males and females and used mate‐guarding duration as our metric of conflict resolution. We discovered that large male posterior gnathopod size increased mate‐guarding duration, which suggests that it is a sexually antagonistic trait in this species. In contrast, female and male body size did not significantly affect mate‐guarding duration. Given that male posterior gnathopods show heightened condition dependence, future investigations should explore the interactive effects of sexual conflict and ecological context on trait evolution, phenotypic divergence, and speciation to elucidate the complex mechanisms involved in the evolution of biological diversity.     

Evolution of the elaborate male intromittent organ of Xiphophorus fishes

Internally fertilizing animals show a remarkable diversity in male genital morphology that is associated with sexual selection, and these traits are thought to be evolving particularly rapidly. Male fish in some internally fertilizing species have “gonopodia,” highly modified anal fins that are putatively important for sexual selection. However, our understanding of the evolution of genital diversity remains incomplete. Contrary to the prediction that male genital traits evolve more rapidly than other traits, here we show that gonopodial traits and other nongonopodial traits exhibit similar evolutionary rates of trait change and also follow similar evolutionary models in an iconic genus of poeciliid fish (Xiphophorus spp.). Furthermore, we find that both mating and nonmating natural selection mechanisms are unlikely to be driving the diverse Xiphophorus gonopodial morphology. Putative holdfast features of the male genital organ do not appear to be influenced by water flow, a candidate selective force in aquatic habitats. Additionally, interspecific divergence in gonopodial morphology is not significantly higher between sympatric species, than between allopatric species, suggesting that male genitals have not undergone reproductive character displacement. Slower rates of evolution in gonopodial traits compared with a subset of putatively sexually selected nongenital traits suggest that different selection mechanisms may be acting on the different trait types. Further investigations of this elaborate trait are imperative to determine whether it is ultimately an important driver of speciation.     

Inferring evolutionary processes from phylogenies

Evolutionary processes shape the regular trends of evolution and are responsible for the diversity and distribution of contemporary species. They include correlated evolutionary change and trajectories of trait evolution, convergent and parallel evolution, differential rates of evolution, speciation and extinction, the order and direction of change in characters, and the nature of the evolutionary process itself—does change accumulate gradually, episodically, or in punctuational bursts. Phylogenies, in combination with information on species, contain the imprint of these historical evolutionary processes. By applying comparative methods based upon statistical models of evolution to well resolved phylogenies, it is possible to infer the historical evolutionary processes that must have existed in the past, given the patterns of diversity seen in the present. I describe a set of maximum likelihood statistical methods for inferring such processes. The methods estimate parameters of statistical models for inferring correlated evolutionary change in continuously varying characters, for detecting correlated evolution in discrete characters, for estimating rates of evolution, and for investigating the nature of the evolutionary process itself. They also anticipate the wealth of information becoming available to biological scientists from genetic studies that pin down relationships among organisms with unprecedented accuracy.     

Adaptive speciation when assortative mating is based on female preference for male marker traits

Adaptive speciation occurs when frequency-dependent ecological interactions generate conditions of disruptive selection to which lineage splitting is an adaptive response. Under such selective conditions, evolution of assortative mating mechanisms enables the break-up of the ancestral lineage into diverging and reproductively isolated descendent species. Extending previous studies, I investigate models of adaptive speciation due to the evolution of indirect assortative mating that is based on three different mating traits: the degree of assortativity, a female preference trait and a male marker trait. For speciation to occur, linkage disequilibria between different mating traits, e.g. between female preference and male marker traits, as well as between mating traits and the ecological trait, must evolve. This can lead to novel speciation scenarios, e.g. when reproductive isolation is generated by a splitting in the degree of assortativeness, with one of the emerging lineages mating assortatively, and the other one disassortatively. I investigate the effects of variation in various model parameters on the likelihood of speciation, as well as robustness of speciation to introducing costs of assortative mating. Even though in the models presented speciation requires the genetic potential for strong assortment as well as rather restrictive ecological conditions, the results show that adaptive speciation due to the evolution of assortative mating when mate choice is based on separate female preference and male marker traits is a theoretically plausible evolutionary scenario.     

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.     

Elevational differentiation accelerates trait evolution but not speciation rates in Amazonian birds

The importance of ecologically mediated divergent selection in accelerating trait evolution has been poorly studied in the most species‐rich biome of the planet, the continental Neotropics. We performed macroevolutionary analyses of trait divergence and diversification rates across closely related pairs of Andean and Amazonian passerine birds, to assess whether the difference in elevational range separating species pairs – a proxy for the degree of ecological divergence – influences the speed of trait evolution and diversification rates. We found that elevational differentiation is associated with faster divergence of song frequency, a trait important for pre‐mating isolation, and several morphological traits, which may contribute to extrinsic post‐mating isolation. However, elevational differentiation did not increase recent speciation rates, possibly due to early bursts of diversification during the uplift of the eastern Andes followed by a slow‐down in speciation rate. Our results suggest that ecological differentiation may speed up trait evolution, but not diversification of Neotropical birds.     

Coping with multiple enemies: pairwise interactions do not predict evolutionary change in complex multitrophic communities

Predicting the ecological and evolutionary trajectories of populations in multispecies communities is one of the fundamental challenges in ecology. Many of these predictions are made by scaling patterns observed from pairwise interactions. Here, we show that the coupling of ecological and evolutionary outcomes is likely to be weaker in increasingly complex communities due to greater chance of life‐history trait correlations. Using model microbial communities comprising a focal bacterial species, Bacillus subtilis, a bacterial competitor, protist predator and phage parasite, we found that increasing the number of enemies in a community had an overall negative effect on B. subtilis population growth. However, only the competitor imposed direct selection for B. subtilis trait evolution in pairwise cultures and this effect was weakened in the presence of other antagonists that had a negative effect on the competitor. In contrast, adaptation to parasites was driven indirectly by correlated selection where competitors had a positive and predators a negative effect. For all measured traits, selection in pairwise communities was a poor predictor of B. subtilis evolution in more complex communities. Together, our results suggest that coupling of ecological and evolutionary outcomes is interaction‐specific and generally less evident in more complex communities where the increasing number of trait correlations could mask weak ecological signals.     

Divergent natural selection promotes immigrant inviability at early and late stages of evolutionary divergence

Natural selection's role in speciation has been of fundamental importance since Darwin first outlined his theory. Recently, work has focused on understanding how selection drives trait divergence, and subsequently reproductive isolation. “Immigrant inviability,” a barrier that arises from selection against immigrants in their nonnative environment, appears to be of particular importance. Although immigrant inviability is likely ubiquitous, we know relatively little about how selection acts on traits to drive immigrant inviability, and how important immigrant inviability is at early‐versus‐late stages of divergence. We present a study evaluating the role of predation in the evolution of immigrant inviability in recently diverged population pairs and a well‐established species pair of Brachyrhaphis fishes. We evaluate performance in a high‐predation environment by assessing survival in the presence of a predator, and swimming endurance in a low‐predation environment. We find strong signatures of local adaptation and immigrant inviability of roughly the same magnitude both early and late in divergence. We find remarkably conserved selection for burst‐speed swimming (important in predator evasion), and selection for increased size in low‐predation environments. Our results highlight the consistency with which selection acts during speciation, and suggest that similar factors might promote initial population differentiation and maintain differentiation at late stages of divergence.     

Sexually antagonistic co‐evolution: a model and an empirical test

Models reveal that sexually antagonistic co‐evolution exaggerates female resistance and male persistence traits. Here we adapt an established model by including directional sexual selection acting against persistence. We find similar equilibria to previous models showing that sexually antagonistic co‐evolution can be limited by counteracting sexual, as well as, natural selection. We tested the model using empirical data for the seaweed fly, Coelopa ursina, in which body size acts as a persistence and a resistance trait. Our model can generate continuous co‐evolutionary cycles and stable equilibria, however, all simulations using empirically derived parameter estimates reach stable equilibria. Thus, stable equilibria might be more common in nature than continuous co‐evolutionary cycles, suggesting that sexual conflict is unlikely to promote speciation. The model predicts male biased sexual size dimorphism for C. ursina, comparable with empirically observed values. Male persistence is shown to be more sensitive than female resistance to changes in model parameters.     

Factors contributing to the accumulation of reproductive isolation: A mixed model approach

The analysis of large datasets describing reproductive isolation between species has been extremely influential in the study of speciation. However, the statistical methods currently used for these data limit the ability to make direct inferences about the factors predicting the evolution of reproductive isolation. As a result, our understanding of iconic patterns and rules of speciation rely on indirect analyses that have clear statistical limitations. Phylogenetic mixed models are commonly used in ecology and evolution, but have not been applied to studies of reproductive isolation. Here I describe a flexible framework using phylogenetic mixed models to analyze data collected at different evolutionary scales, to test both categorical and continuous predictor variables, and to test the effect of multiple predictors on rates and patterns of reproductive isolation simultaneously. I demonstrate the utility of this framework by re‐analyzing four classic datasets, from both animals and plants, and evaluating several hypotheses that could not be tested in the original studies: In the Drosophila and Bufonidae datasets, I found support for more rapid accumulation of reproductive isolation in sympatric species pairs compared to allopatric species pairs. Using Silene and Nolana, I found no evidence supporting the hypothesis that floral differentiation elevates postzygotic reproductive isolation. The faster accumulation of postzygotic isolation in sympatry is likely the result of species coexistence determined by the level of postzygotic isolation between species. In addition, floral trait divergence does not appear to translate into pleiotropic effects on postzygotic reproductive isolation. Overall, these methods can allow researchers to test new hypotheses using a single statistical method, while remedying the statistical limitations of several previous methods.     

How traits shape trees: new approaches for detecting character state‐dependent lineage diversification

Biologists have long sought to understand the processes underlying disparities in clade size across the tree of life and the extent to which such clade size differences can be attributed to the evolution of particular traits. The association of certain character states with species‐rich clades suggests that trait evolution can lead to increased diversification, but such a pattern could also arise due other processes, such as directional trait evolution. Recent advances in phylogenetic comparative methods have provided new statistical approaches for distinguishing between these intertwined and potentially confounded macroevolutionary processes. Here, we review the historical development of methods for detecting state‐dependent diversification and explore what new methods have revealed about classic examples of traits that affect diversification, including evolutionary dead ends, key innovations and geographic traits. Applications of these methods thus far collectively suggest that trait diversity commonly arises through the complex interplay between transition, speciation and extinction rates and that long hypothesized evolutionary dead ends and key innovations are instead often cases of directional trends in trait evolution.     

Relating traits to diversification: a simple test

We describe a simple comparative method for determining whether rates of diversification are correlated with continuous traits in species-level phylogenies. This involves comparing traits of species with net speciation rate (number of nodes linking extant species with the root divided by the root to tip evolutionary distance), using a phylogenetically corrected correlation. We use simulations to examine the power of this test. We find that the approach has acceptable power to uncover relationships between speciation and a continuous trait and is robust to background random extinction; however, the power of the approach is reduced when the rate of trait evolution is decreased. The test has low power to relate diversification to traits when extinction rate is correlated with the trait. Clearly, there are inherent limitations in using only data on extant species to infer correlates of extinction; however, this approach is potentially a powerful tool in analyzing correlates of speciation.     

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.     

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.