Showing papers in "Evolution in 2016"
TL;DR: Several ways in which the possible presence of hemiplasy can be diagnosed are offered, and multiple approaches to dealing with the problems presented by underlying gene tree discordance when carrying out character mapping are discussed.
Abstract: Phylogenomics has largely succeeded in its aim of accurately inferring species trees, even when there are high levels of discordance among individual gene trees. These resolved species trees can be used to ask many questions about trait evolution, including the direction of change and number of times traits have evolved. However, the mapping of traits onto trees generally uses only a single representation of the species tree, ignoring variation in the gene trees used to construct it. Recognizing that genes underlie traits, these results imply that many traits follow topologies that are discordant with the species topology. As a consequence, standard methods for character mapping will incorrectly infer the number of times a trait has evolved. This phenomenon, dubbed "hemiplasy," poses many problems in analyses of character evolution. Here we outline these problems, explaining where and when they are likely to occur. We offer several ways in which the possible presence of hemiplasy can be diagnosed, and discuss multiple approaches to dealing with the problems presented by underlying gene tree discordance when carrying out character mapping. Finally, we discuss the implications of hemiplasy for general phylogenetic inference, including the possible drawbacks of the widespread push for "resolved" species trees.
182 citations
TL;DR: The data suggest that anoles in urban areas are under significant differential natural selection and may be evolutionarily adapting to their human‐modified environments.
Abstract: Urbanization is an increasingly important dimension of global change, and urban areas likely impose significant natural selection on the species that reside within them. Although many species of plants and animals can survive in urban areas, so far relatively little research has investigated whether such populations have adapted (in an evolutionary sense) to their newfound milieu. Even less of this work has taken place in tropical regions, many of which have experienced dramatic growth and intensification of urbanization in recent decades. In the present study, we focus on the neotropical lizard, Anolis cristatellus. We tested whether lizard ecology and morphology differ between urban and natural areas in three of the most populous municipalities on the island of Puerto Rico. We found that environmental conditions including temperature, humidity, and substrate availability differ dramatically between neighboring urban and natural areas. We also found that lizards in urban areas use artificial substrates a large proportion of the time, and that these substrates tend to be broader than substrates in natural forest. Finally, our morphological data showed that lizards in urban areas have longer limbs relative to their body size, as well as more subdigital scales called lamellae, when compared to lizards from nearby forested habitats. This shift in phenotype is exactly in the direction predicted based on habitat differences between our urban and natural study sites, combined with our results on how substrates are being used by lizards in these areas. Findings from a common-garden rearing experiment using individuals from one of our three pairs of populations provide evidence that trait differences between urban and natural sites may be genetically based. Taken together, our data suggest that anoles in urban areas are under significant differential natural selection and may be evolutionarily adapting to their human-modified environments.
162 citations
TL;DR: A standardized test statistic (a z‐score) is proposed for measuring the degree of morphological integration between sets of variables, based on a partial least squares analysis of trait covariation, and its permutation‐based sampling distribution.
Abstract: Evolutionary morphologists frequently wish to understand the extent to which organisms are integrated, and whether the strength of morphological integration among subsets of phenotypic variables differ among taxa or other groups. However, comparisons of the strength of integration across datasets are difficult, in part because the summary measures that characterize these patterns (RV coefficient and rPLS ) are dependent both on sample size and on the number of variables. As a solution to this issue, we propose a standardized test statistic (a z-score) for measuring the degree of morphological integration between sets of variables. The approach is based on a partial least squares analysis of trait covariation, and its permutation-based sampling distribution. Under the null hypothesis of a random association of variables, the method displays a constant expected value and confidence intervals for datasets of differing sample sizes and variable number, thereby providing a consistent measure of integration suitable for comparisons across datasets. A two-sample test is also proposed to statistically determine whether levels of integration differ between datasets, and an empirical example examining cranial shape integration in Mediterranean wall lizards illustrates its use. Some extensions of the procedure are also discussed.
129 citations
TL;DR: It is found that modest levels of heterogeneity in speciation rate result in a consistent, positive bias in extinction estimates that are exacerbated by phylogenetic tree size, and suggests that extinction rate estimates from phylogenies of extant taxa only should be treated with caution.
Abstract: Time-calibrated phylogenies that contain only living species have been widely used to study the dynamics of speciation and extinction. Concerns about the reliability of phylogenetic extinction estimates were raised by Rabosky (2010), where I suggested that unaccommodated heterogeneity in speciation rate could lead to positively biased extinction estimates. In a recent article, Beaulieu and O'Meara (2015a) correctly point out several technical errors in the execution of my 2010 study and concluded that phylogenetic extinction estimates are robust to speciation rate heterogeneity under a range of model parameters. I demonstrate that Beaulieu and O'Meara underestimated the magnitude of speciation rate variation in real phylogenies and consequently did not incorporate biologically meaningful levels of rate heterogeneity into their simulations. Using parameter values drawn from the recent literature, I find that modest levels of heterogeneity in speciation rate result in a consistent, positive bias in extinction estimates that are exacerbated by phylogenetic tree size. This bias, combined with the inherent lack of information about extinction in molecular phylogenies, suggests that extinction rate estimates from phylogenies of extant taxa only should be treated with caution.
93 citations
TL;DR: Infected flies exposed to cold conditions for an extended period had reduced fecundity and viability, an effect not evident in unexposed controls, whereas different processes, including CI induced by young males, may contribute to higher frequencies in tropical locations.
Abstract: Field populations of arthropods are often polymorphic for Wolbachia but the factors maintaining intermediate Wolbachia frequencies are generally not understood. In Drosophila melanogaster, Wolbachia frequencies are highly variable across the globe. We document the persistence of a Wolbachia infection frequency cline in D. melanogaster populations from eastern Australia across at least 20 years, with frequencies generally high in the tropics but lower in cool temperate regions. The results are interpreted using a model of frequency dynamics incorporating cytoplasmic incompatibility (CI), imperfect maternal transmission and Wolbachia effects on fitness. Clinal variation is less pronounced in eastern North America which may reflect annual recolonization at higher latitudes. Limited samples from Africa from latitudes matching our tropical and subtropical samples from Australia and North America show comparably high infection frequencies, but some equatorial samples show lower frequencies. Adult dormancy across cold periods may contribute to the Australian Wolbachia cline. Infected flies exposed to cold conditions for an extended period had reduced fecundity and viability, an effect not evident in unexposed controls. These fitness costs may contribute to the relatively low Wolbachia frequencies in Australian temperate areas; whereas different processes, including CI induced by young males, may contribute to higher frequencies in tropical locations.
93 citations
TL;DR: This work uses a single‐locus model to examine how MGEs contribute patterns of heritable and nonheritable variation and influence evolutionary dynamics in randomly mating and inbreeding populations and shows that additive and dominance M GEs make different contributions to evolutionary dynamics and patterns of variation.
Abstract: Maternal genetic effects (MGEs), where genes expressed by mothers affect the phenotype of their offspring, are important sources of phenotypic diversity in a myriad of organisms. We use a single-locus model to examine how MGEs contribute patterns of heritable and nonheritable variation and influence evolutionary dynamics in randomly mating and inbreeding populations. We elucidate the influence of MGEs by examining the offspring genotype-phenotype relationship, which determines how MGEs affect evolutionary dynamics in response to selection on offspring phenotypes. This approach reveals important results that are not apparent from classic quantitative genetic treatments of MGEs. We show that additive and dominance MGEs make different contributions to evolutionary dynamics and patterns of variation, which are differentially affected by inbreeding. Dominance MGEs make the offspring genotype-phenotype relationship frequency dependent, resulting in the appearance of negative frequency-dependent selection, while additive MGEs contribute a component of parent-of-origin dependent variation. Inbreeding amplifies the contribution of MGEs to the additive genetic variance and, therefore enhances their evolutionary response. Considering evolutionary dynamics of allele frequency change on an adaptive landscape, we show that this landscape differs from the mean fitness surface, and therefore, under some condition, fitness peaks can exist but not be "available" to the evolving population.
86 citations
TL;DR: A maximum likelihood approach that takes into account model parameterization is presented, allowing for the direct comparison of models with different parameterizations, providing an important tool for the analysis of modularity across diverse systems.
Abstract: Identification of phenotypic modules, semi-autonomous sets of highly-correlated traits, can be accomplished through exploratory (e.g., cluster analysis) or confirmatory approaches (e.g., RV coefficient analysis). While statistically more robust, confirmatory approaches are generally unable to compare across different model structures. For example, RV coefficient analysis finds support for both two- and six-module models for the therian mammalian skull. Here, we present a maximum likelihood approach that takes into account model parameterization. We compare model log-likelihoods of trait correlation matrices using the finite-sample corrected Akaike Information Criterion, allowing for comparison of hypotheses across different model structures. Simulations varying model complexity and within- and between-module contrast demonstrate that this method correctly identifies model structure and parameters across a wide range of conditions. We further analyzed a dataset of 3-D data, consisting of 61 landmarks from 181 macaque (Macaca fuscata) skulls, distributed among five age categories, testing 31 models, including no modularity among the landmarks, and various partitions of 2, 3, 6, and 8 modules. Our results clearly support a complex six-module model, with separate within- and inter-module correlations. Furthermore, this model was selected for all five age categories, demonstrating that this complex pattern of integration in the macaque skull appears early and is highly conserved throughout postnatal ontogeny. Subsampling analyses demonstrate that this method is robust to relatively low sample sizes, as is commonly encountered in rare or extinct taxa. This new approach allows for the direct comparison of models with different parameterizations, providing an important tool for the analysis of modularity across diverse systems. This article is protected by copyright. All rights reserved.
79 citations
TL;DR: The results illustrate that the extent of river branching, confluence position, and levels of asymmetric downstream migration dictate patterns of genetic variation in riverine populations and highlight the importance of incorporating riverscape information into evolutionary models of aquatic species.
Abstract: It is widely recognized that physical landscapes can shape genetic variation within and between populations. However, it is not well understood how riverscapes, with their complex architectures, affect patterns of neutral genetic diversity. Using a spatially explicit agent-based modeling (ABM) approach, we evaluate the genetic consequences of dendritic river shapes on local population structure. We disentangle the relative contribution of specific river properties to observed patterns of genetic variation by evaluating how different branching architectures and downstream flow regimes affect the genetic structure of populations situated within river networks. Irrespective of the river length, our results illustrate that the extent of river branching, confluence position, and levels of asymmetric downstream migration dictate patterns of genetic variation in riverine populations. Comparisons between simple and highly branched rivers show a 20-fold increase in the overall genetic diversity and a sevenfold increase in the genetic differentiation between local populations. Given that most rivers have complex architectures, these results highlight the importance of incorporating riverscape information into evolutionary models of aquatic species and could help explain why riverine fishes represent a disproportionately large amount of global vertebrate diversity per unit of habitable area.
73 citations
TL;DR: This work ascertain uninvadability (all mutant strategies always go extinct) in terms of the asymptotic per capita number of mutant copies produced by a mutant lineage arising as a single copy in a resident population (“invasion fitness”).
Abstract: How should fitness be measured to determine which phenotype or "strategy" is uninvadable when evolution occurs in a group-structured population subject to local demographic and environmental heterogeneity? Several fitness measures, such as basic reproductive number, lifetime dispersal success of a local lineage, or inclusive fitness have been proposed to address this question, but the relationships between them and their generality remains unclear. Here, we ascertain uninvadability (all mutant strategies always go extinct) in terms of the asymptotic per capita number of mutant copies produced by a mutant lineage arising as a single copy in a resident population ("invasion fitness"). We show that from invasion fitness uninvadability is equivalently characterized by at least three conceptually distinct fitness measures: (i) lineage fitness, giving the average individual fitness of a randomly sampled mutant lineage member; (ii) inclusive fitness, giving a reproductive value weighted average of the direct fitness costs and relatedness weighted indirect fitness benefits accruing to a randomly sampled mutant lineage member; and (iii) basic reproductive number (and variations thereof) giving lifetime success of a lineage in a single group, and which is an invasion fitness proxy. Our analysis connects approaches that have been deemed different, generalizes the exact version of inclusive fitness to class-structured populations, and provides a biological interpretation of natural selection on a mutant allele under arbitrary strength of selection.
72 citations
TL;DR: It is shown that there is a very simple and general reason why unequal gamete numbers result in unequal investment in sexually competitive traits, and sex roles thus ultimately trace back to anisogamy and the resulting consequences for the fertilization process.
Abstract: There is a clear tendency in nature for males to compete more strongly for fertilizations than females, yet the ultimate reasons for this are still unclear. Many researchers-dating back to Darwin and Bateman-have argued that the difference is ultimately driven by the fact that males (by definition) produce smaller and more numerous gametes than females. However, this view has recently been challenged, and a formal validation of the link between anisogamy and sex roles has been lacking. Here, we develop mathematical models that validate the intuition of Darwin and Bateman, showing that there is a very simple and general reason why unequal gamete numbers result in unequal investment in sexually competitive traits. This asymmetry does not require multiple mating by either sex, and covers traits such as mate searching, where the male bias has been difficult to explain. Furthermore, our models show males and females are predicted to diverge more strongly when the fertilization probability of each female gamete is high. Sex roles thus ultimately trace back to anisogamy and the resulting consequences for the fertilization process.
67 citations
TL;DR: The results demonstrate that male reproductive success in M. lignano is not primarily limited by the number of matings achieved, but rather by the ability to convert matings into successful fertilizations, which is facilitated by producing many sperm.
Abstract: Sexual selection operates through consecutive episodes of selection that ultimately contribute to the observed variance in reproductive success between individuals. Understanding the relative importance of these episodes is challenging, particularly because the relevant postcopulatory fitness components are often difficult to assess. Here, we investigate different episodes of sexual selection on the male sex function, by assessing how (precopulatory) mating success, and (postcopulatory) sperm-transfer efficiency and sperm-fertilizing efficiency contribute to male reproductive success. Specifically, we used a transgenic line of the transparent flatworm, Macrostomum lignano, which expresses green fluorescent protein (GFP) in all cell types, including sperm cells, enabling in vivo sperm tracking and paternity analysis. We found that a large proportion of variance in male reproductive success arose from the postcopulatory episodes. Moreover, we also quantified selection differentials on 10 morphological traits. Testis size and seminal vesicle size showed significant positive selection differentials, which were mainly due to selection on sperm-transfer efficiency. Overall, our results demonstrate that male reproductive success in M. lignano is not primarily limited by the number of matings achieved, but rather by the ability to convert matings into successful fertilizations, which is facilitated by producing many sperm.
TL;DR: This work simplifies previous computational descriptions of PGLS standard errors in a manner that can be easily generalized toward more complex general linear models and focuses on the implementation of phylogenetic analysis of covariance, which provides a direct test for the equality of intercepts and slopes.
Abstract: Phylogenetic generalized least squares (PGLS) has become one of the most commonly used phylogenetic comparative methods. Despite its common use, descriptions, and applications of methods to test for species' deviations from allometric predictions using phylogenetic regression have been piecemeal. We simplify previous computational descriptions of PGLS standard errors in a manner that can be easily generalized toward more complex general linear models. We focus on the implementation of phylogenetic analysis of covariance, which provides a direct test for the equality of intercepts and slopes. Our computational descriptions allow testing whether individual species, or a group of species, deviate significantly from allometric predictions. The use of PGLS confidence and prediction intervals and phylogenetic analysis of covariance is exemplified in an analysis of brain structure volumes in primates.
TL;DR: It is demonstrated that microhabitat has driven wing shape evolution, although it has not strongly affected forewing and hindwing integration, and it is found that sexual dimorphism of forewing shape and color pattern are coupled, suggesting a common selective force.
Abstract: Butterfly wings harbor highly diverse phenotypes and are involved in many functions. Wing size and shape result from interactions between adaptive processes, phylogenetic history, and developmental constraints, which are complex to disentangle. Here, we focus on the genus Morpho (Nymphalidae: Satyrinae, 30 species), which presents a high diversity of sizes, shapes, and color patterns. First, we generate a comprehensive molecular phylogeny of these 30 species. Next, using 911 collection specimens, we quantify the variation of wing size and shape across species, to assess the importance of shared ancestry, microhabitat use, and sexual selection in the evolution of the wings. While accounting for phylogenetic and allometric effects, we detect a significant difference in wing shape but not size among microhabitats. Fore and hindwings covary at the individual and species levels, and the covariation differs among microhabitats. However, the microhabitat structure in covariation disappears when phylogenetic relationships are taken into account. Our results demonstrate that microhabitat has driven wing shape evolution, although it has not strongly affected forewing and hindwing integration. We also found that sexual dimorphism of forewing shape and color pattern are coupled, suggesting a common selective force.
TL;DR: It is found that environmental change often aligns directional selection between the sexes, even when they have divergent phenotypic optima, and generates new predictions regarding the scope for sexually antagonistic selection and its resolution in changing environments.
Abstract: Females and males have conflicting evolutionary interests. Selection favors the evolution of different phenotypes within each sex, yet divergence between the sexes is constrained by the shared genetic basis of female and male traits. Current theory predicts that such "sexual antagonism" should be common: manifesting rapidly during the process of adaptation, and slow in its resolution. However, these predictions apply in temporally stable environments. Environmental change has been shown empirically to realign the direction of selection acting on shared traits and thereby alleviate signals of sexually antagonistic selection. Yet there remains no theory for how common sexual antagonism should be in changing environments. Here, we analyze models of sex-specific evolutionary divergence under directional and cyclic environmental change, and consider the impact of genetic correlations on long-run patterns of sex-specific adaptation. We find that environmental change often aligns directional selection between the sexes, even when they have divergent phenotypic optima. Nevertheless, some forms of environmental change generate persistent sexually antagonistic selection that is difficult to resolve. Our results reinforce recent empirical observations that changing environmental conditions alleviate conflict between males and females. They also generate new predictions regarding the scope for sexually antagonistic selection and its resolution in changing environments.
TL;DR: The results demonstrate that flower color traits influence pollination success and seed production in A. morio, indicating that they affect attractiveness to pollinators, efficiency of pollen transfer, or both.
Abstract: Contrasting flower color patterns that putatively attract or direct pollinators toward a reward are common among angiosperms. In the deceptive orchid Anacamptis morio, the lower petal, which makes ...
TL;DR: This work derives the expected levels of gene diversity within populations and divergence between them for male sperm protein genes evolving by postcopulatory, prezygotic fertility competition, i.e. the function imputed for some sperm and seminal fluid genes and finds that they are elevated relative to genes with similar selection coefficients expressed by both sexes.
Abstract: It is widely established that proteins involved in reproduction diverge between species more quickly than other proteins. For male sperm proteins, rapid divergence is believed to be caused by postcopulatory sexual selection and/or sexual conflict. Here, we derive the expected levels of gene diversity within populations and divergence between them for male sperm protein genes evolving by postcopulatory, prezygotic fertility competition, i.e. the function imputed for some sperm and seminal fluid genes. We find that, at the mutation-selection equilibrium, both gene diversity within species and divergence between them are elevated relative to genes with similar selection coefficients expressed by both sexes. We show that their expected level of diversity is a function of the harmonic mean number of mates per female, which affects the strength of fertility selection stemming from male-male sperm competition. Our predictions provide a null hypothesis for distinguishing between other selective hypotheses accounting for the rapid evolution of male reproductive genes.
TL;DR: It is shown that, with a few modifications, Fisher's model can generate all of the major findings of introgression studies, including “speciation genes” with strong deleterious effects, complex epistasis and asymmetry, and the major patterns in overall hybrid fitnesses.
Abstract: Research in speciation genetics has uncovered many robust patterns in intrinsic reproductive isolation, and fitness landscape models have been useful in interpreting these patterns. Here, we examine fitness landscapes based on Fisher's geometric model. Such landscapes are analogous to models of optimizing selection acting on quantitative traits, and have been widely used to study adaptation and the distribution of mutational effects. We show that, with a few modifications, Fisher's model can generate all of the major findings of introgression studies (including "speciation genes" with strong deleterious effects, complex epistasis and asymmetry), and the major patterns in overall hybrid fitnesses (including Haldane's Rule, the speciation clock, heterosis, hybrid breakdown, and male-female asymmetry in the F1). We compare our approach to alternative modeling frameworks that assign fitnesses to genotypes by identifying combinations of incompatible alleles. In some cases, the predictions are importantly different. For example, Fisher's model can explain conflicting empirical results about the rate at which incompatibilities accumulate with genetic divergence. In other cases, the predictions are identical. For example, the quality of reproductive isolation is little affected by the manner in which populations diverge.
TL;DR: This work combines experimental evolution and partial genome resequencing of replicate seed beetle selection lines to test the trade‐off hypothesis and measure the repeatability of evolution, finding that some alleles that were favored on lentil were selected against during reversion on mung bean, consistent with the genetic trade‐offs hypothesis.
Abstract: Trade-offs have often been invoked to explain the evolution of ecological specialization. Phytophagous insects have been especially well studied, but there has been little evidence that resource-based trade-offs contribute to the evolution of host specialization in this group. Here, we combine experimental evolution and partial genome resequencing of replicate seed beetle selection lines to test the trade-off hypothesis and measure the repeatability of evolution. Bayesian estimates of selection coefficients suggest that rapid adaptation to a poor host (lentil) was mediated by standing genetic variation at multiple genetic loci and involved many of the same variants in replicate lines. Sublines that were then switched back to the ancestral host (mung bean) showed a more gradual and variable (less repeatable) loss of adaptation to lentil. We were able to obtain estimates of variance effective population sizes from genome-wide differences in allele frequencies within and between lines. These estimates were relatively large, which suggests that the contribution of genetic drift to the loss of adaptation following reversion was small. Instead, we find that some alleles that were favored on lentil were selected against during reversion on mung bean, consistent with the genetic trade-off hypothesis.
TL;DR: This study provides the strongest comparative support to date for both the energetic trade‐off and the behavioral flexibility hypotheses, and highlights that both mechanisms contribute to brain size evolution, but on different ends of the migratory spectrum.
Abstract: Brain size relative to body size is smaller in migratory than in nonmigratory birds. Two mutually nonexclusive hypotheses had been proposed to explain this association. On the one hand, the "energetic trade-off hypothesis" claims that migratory species were selected to have smaller brains because of the interplay between neural tissue volume and migratory flight. On the other hand, the "behavioral flexibility hypothesis" argues that resident species are selected to have higher cognitive capacities, and therefore larger brains, to enable survival in harsh winters, or to deal with environmental seasonality. Here, I test the validity and setting of these two hypotheses using 1466 globally distributed bird species. First, I show that the negative association between migration distance and relative brain size is very robust across species and phylogeny. Second, I provide strong support for the energetic trade-off hypothesis, by showing the validity of the trade-off among long-distance migratory species alone. Third, using resident and short-distance migratory species, I demonstrate that environmental harshness is associated with enlarged relative brain size, therefore arguably better cognition. My study provides the strongest comparative support to date for both the energetic trade-off and the behavioral flexibility hypotheses, and highlights that both mechanisms contribute to brain size evolution, but on different ends of the migratory spectrum.
TL;DR: Comparisons of fine‐scale population structure in codistributed Zelandoperla stonefly species, across three parallel altitudinal transects in New Zealand's Rock and Pillar mountain range, support the hypothesis that wing‐loss can initiate diversification in alpine insect populations over small spatial scales.
Abstract: Insect flight loss is a repeated phenomenon in alpine habitats, where wing reduction is thought to enhance local recruitment and increase fecundity. One predicted consequence of flight loss is reduced dispersal ability, which should lead to population genetic differentiation and perhaps ultimately to speciation. Using a dataset of 15,123 SNP loci, we present comparative analyses of fine-scale population structure in codistributed Zelandoperla stonefly species, across three parallel altitudinal transects in New Zealand's Rock and Pillar mountain range. We find that winged populations (altitude 200-500 m; Zelandoperla decorata) show no genetic structuring within or among streams, suggesting substantial dispersal mediated by flight. By contrast, wingless populations (Zelandoperla fenestrata; altitude 200-1100 m) exhibit distinct genetic clusters associated with each stream, and additional evidence of isolation by distance within streams. Our data support the hypothesis that wing-loss can initiate diversification in alpine insect populations over small spatial scales. The often deep phylogenetic placement of lowland Z. fenestrata within their stream-specific clades suggests the possibility of independent alpine colonization events for each stream. Additionally, the detection of winged, interspecific hybrid individuals raises the intriguing possibility that a previously flightless lineage could reacquire flight via introgression.
TL;DR: A comprehensive phylogenetic analysis of carnivorous murids of the IAA demonstrates that carnivory evolved independently four times after overwater colonization, including in situ origins on the Philippines, Sulawesi, and Sahul.
Abstract: Convergent evolution, often observed in island archipelagos, provides compelling evidence for the importance of natural selection as a generator of species and ecological diversity. The Indo-Australian Archipelago (IAA) is the world's largest island system and encompasses distinct biogeographic units, including the Asian (Sunda) and Australian (Sahul) continental shelves, which together bracket the oceanic archipelagos of the Philippines and Wallacea. Each of these biogeographic units houses numerous endemic rodents in the family Muridae. Carnivorous murids, that is those that feed on animals, have evolved independently in Sunda, Sulawesi (part of Wallacea), the Philippines, and Sahul, but the number of origins of carnivory among IAA murids is unknown. We conducted a comprehensive phylogenetic analysis of carnivorous murids of the IAA, combined with estimates of ancestral states for broad diet categories (herbivore, omnivore, and carnivore) and geographic ranges. These analyses demonstrate that carnivory evolved independently four times after overwater colonization, including in situ origins on the Philippines, Sulawesi, and Sahul. In each biogeographic unit the origin of carnivory was followed by evolution of more specialized carnivorous ecomorphs such as vermivores, insectivores, and amphibious rats.
TL;DR: It is demonstrated that physiological parameters are either associated with changes in local thermal habitat or to basking behavior, but not both, and distinct responses among traits indicate the multiple selective pressures and constraints that shape the evolution of thermal performance.
Abstract: There is pressing urgency to understand how tropical ectotherms can behaviorally and physiologically respond to climate warming. We examine how basking behavior and thermal environment interact to influence evolutionary variation in thermal physiology of multiple species of lygosomine rainforest skinks from the Wet Tropics of northeastern Queensland, Australia (AWT). These tropical lizards are behaviorally specialized to exploit canopy or sun, and are distributed across marked thermal clines in the AWT. Using phylogenetic analyses, we demonstrate that physiological parameters are either associated with changes in local thermal habitat or to basking behavior, but not both. Cold tolerance, the optimal sprint speed, and performance breadth are primarily influenced by local thermal environment. Specifically, montane lizards are more cool tolerant, have broader performance breadths, and higher optimum sprinting temperatures than their lowland counterparts. Heat tolerance, in contrast, is strongly affected by basking behavior: there are two evolutionary optima, with basking species having considerably higher heat tolerance than shade skinks, with no effect of elevation. These distinct responses among traits indicate the multiple selective pressures and constraints that shape the evolution of thermal performance. We discuss how behavior and physiology interact to shape organisms’ vulnerability and potential resilience to climate change.
TL;DR: There appear to be few constraints on fish emerging onto land given amphibious behavior has evolved repeatedly many times across ecologically diverse families, providing an important prerequisite for subsequent adaptive differentiation.
Abstract: We know little about on how frequently transitions into new habitats occur, especially the colonization of novel environments that are the most likely to instigate adaptive evolution. One of the most extreme ecological transitions has been the shift in habitat associated with the move from water to land by amphibious fish. We provide the first phylogenetic investigation of these transitions for living fish. Thirty-three families have species reported to be amphibious and these are likely independent evolutionary origins of fish emerging onto land. Phylogenetic reconstructions of closely related taxa within one of these families, the Blenniidae, inferred as many as seven convergences on a highly amphibious lifestyle. Taken together, there appear to be few constraints on fish emerging onto land given amphibious behavior has evolved repeatedly many times across ecologically diverse families. The colonization of novel habitats by other taxa resulting in less dramatic changes in environment should be equally, if not, more frequent in nature, providing an important prerequisite for subsequent adaptive differentiation.
TL;DR: By reconstructing the most complete molecular phylogeny of African Bufonidae to date, it is found that the diversification of lineages in Africa best conforms to a constant rate model throughout time and across subclades, with little support for EO.
Abstract: The niche-filling process predicted by the “ecological opportunity” (EO) model is an often-invoked mechanism for generating exceptional diversity in island colonizers. Whether the same process governs lineage accumulation and trait disparity during continental colonization events is less clear. Here, we test this prediction by investigating the rate dynamics and trait evolution of one of Africa's most widespread amphibian colonizers, the true toads (Bufonidae). By reconstructing the most complete molecular phylogeny of African Bufonidae to date, we find that the diversification of lineages in Africa best conforms to a constant rate model throughout time and across subclades, with little support for EO. Evolutionary rates of life-history traits have similarly been constant over time. However, an analysis of generalists and specialists showed a shift toward higher speciation rates associated with habitat specialization. The overall lack of EO signal can be interpreted in a number of ways and we propose several explanations. Firstly, methodological issues might preclude the detection of EO. Secondly, colonizers might not experience true EO conditions and due to the size, ecological heterogeneity and age of landmasses, the diversification processes might be more complex. Thirdly, lower speciation rates of habitat generalists may have affected overall proliferation of lineages.
TL;DR: This article comprehensively test for reproductive isolation between recently diverged dune and nondune ecotypes of the prairie sunflower, Helianthus petiolaris, and finds reproductive barriers acting at multiple stages of hybridization, including premating, postmating–prezygotic, and postzyGotic barriers, despite the recent divergence.
Abstract: Measuring reproductive barriers between groups of organisms is an effective way to determine the traits and mechanisms that impede gene flow. However, to understand the ecological and evolutionary factors that drive speciation, it is important to distinguish between the barriers that arise early in the speciation process and those that arise after speciation is largely complete. In this article, we comprehensively test for reproductive isolation between recently diverged (<10,000 years bp) dune and nondune ecotypes of the prairie sunflower, Helianthus petiolaris. We find reproductive barriers acting at multiple stages of hybridization, including premating, postmating-prezygotic, and postzygotic barriers, despite the recent divergence. Barriers include extrinsic selection against immigrants and hybrids, a shift in pollinator assemblage, and postpollination assortative mating. Together, these data suggest that multiple barriers can be important for reducing gene flow in the earliest stages of speciation.
TL;DR: Analysis of geographic SSD variation in closely related black scavenger flies revealed at least six independent origins of male‐biased SSD in Sepsidae, which is likely caused by sexual selection on male size and mediated by bimaturism.
Abstract: Sexual size dimorphism (SSD) arises when the net effects of natural and sexual selection on body size differ between the sexes Quantitative SSD variation between taxa is common, but directional intraspecific SSD reversals are rare We combined micro- and macroevolutionary approaches to study geographic SSD variation in closely related black scavenger flies Common garden experiments revealed stark intra- and interspecific variation: Sepsis biflexuosa is monomorphic across the Holarctic, while S cynipsea (only in Europe) consistently exhibits female-biased SSD Interestingly, S neocynipsea displays contrasting SSD in Europe (females larger) and North America (males larger), a pattern opposite to the geographic reversal in SSD of S punctum documented in a previous study In accordance with the differential equilibrium model for the evolution of SSD, the intensity of sexual selection on male size varied between continents (weaker in Europe), whereas fecundity selection on female body size did not Subsequent comparative analyses of 49 taxa documented at least six independent origins of male-biased SSD in Sepsidae, which is likely caused by sexual selection on male size and mediated by bimaturism Therefore, reversals in SSD and the associated changes in larval development might be much more common and rapid and less constrained than currently assumed
TL;DR: It is shown how mixed model‐based approaches can provide more robust inferences than more commonly used multistep statistical approaches, and derive new metrics of the relative importance of variation in reaction norm intercepts, slopes, and curvatures.
Abstract: Analysis of reaction norms, the functions by which the phenotype produced by a given genotype depends on the environment, is critical to studying many aspects of phenotypic evolution. Different techniques are available for quantifying different aspects of reaction norm variation. We examine what biological inferences can be drawn from some of the more readily applicable analyses for studying reaction norms. We adopt a strongly biologically motivated view, but draw on statistical theory to highlight strengths and drawbacks of different techniques. In particular, consideration of some formal statistical theory leads to revision of some recently, and forcefully, advocated opinions on reaction norm analysis. We clarify what simple analysis of the slope between mean phenotype in two environments can tell us about reaction norms, explore the conditions under which polynomial regression can provide robust inferences about reaction norm shape, and explore how different existing approaches may be used to draw inferences about variation in reaction norm shape. We show how mixed model-based approaches can provide more robust inferences than more commonly used multistep statistical approaches, and derive new metrics of the relative importance of variation in reaction norm intercepts, slopes, and curvatures.
TL;DR: It is demonstrated that a reproductive barrier acts after copulation but before fertilization in a socially monogamous vertebrate, and it is implied that there is opportunity for it to be accentuated via a reinforcement‐like process.
Abstract: When hybridization is maladaptive, species-specific mate preferences are selectively favored, but low mate availability may constrain species-assortative pairing. Females paired to heterospecifics may then benefit by copulating with multiple males and subsequently favoring sperm of conspecifics. Whether such mechanisms for biasing paternity toward conspecifics act as important reproductive barriers in socially monogamous vertebrate species remains to be determined. We use a combination of long-term breeding records from a natural hybrid zone between collared and pied flycatchers (Ficedula albicollis and F. hypoleuca), and an in vitro experiment comparing conspecific and heterospecific sperm performance in female reproductive tract fluid, to evaluate the potential significance of female cryptic choice. We show that the females most at risk of hybridizing (pied flycatchers) frequently copulate with multiple males and are able to inhibit heterospecific sperm performance. The negative effect on heterospecific sperm performance was strongest in pied flycatcher females that were most likely to have been previously exposed to collared flycatcher sperm. We thus demonstrate that a reproductive barrier acts after copulation but before fertilization in a socially monogamous vertebrate. While the evolutionary history of this barrier is unknown, our results imply that there is opportunity for it to be accentuated via a reinforcement-like process.
TL;DR: The results suggest that reproductive isolation between these three populations is almost complete despite the absence of geographic barriers, and that the main drivers of this isolation are ecologically based, consistent with the mechanisms underlying ecological speciation.
Abstract: Speciation proceeds when gene exchange is prevented between populations. Determining the different barriers preventing gene flow can therefore give insights into the factors driving and maintaining species boundaries. These reproductive barriers may result from intrinsic genetic incompatibilities between populations, from extrinsic environmental differences between populations, or a combination of both mechanisms. We investigated the potential barriers to gene exchange between three adjacent ecotypes of an Australian wildflower to determine the strength of individual barriers and the degree of overall isolation between populations. We found almost complete isolation between the three populations mainly due to premating extrinsic barriers. Intrinsic genetic barriers were weak and variable among populations. There were asymmetries in some intrinsic barriers due to the origin of cytoplasm in hybrids. Overall, these results suggest that reproductive isolation between these three populations is almost complete despite the absence of geographic barriers, and that the main drivers of this isolation are ecologically based, consistent with the mechanisms underlying ecological speciation.
TL;DR: By describing how ecological speciation likely occurs more readily at high latitudes, with such nascent species especially prone to extinction by fusion, the ephemeral ecological speciating hypothesis is derived as an integrative mechanistic explanation for latitudinal gradients in species turnover and the net accumulation of biodiversity.
Abstract: The richness of biodiversity in the tropics compared to high-latitude parts of the world forms one of the most globally conspicuous patterns in biology, and yet few hypotheses aim to explain this phenomenon in terms of explicit microevolutionary mechanisms of speciation and extinction. We link population genetic processes of selection and adaptation to speciation and extinction by way of their interaction with environmental factors to drive global scale macroecological patterns. High-latitude regions are both cradle and grave with respect to species diversification. In particular, we point to a conceptual equivalence of "environmental harshness" and "hard selection" as eco-evolutionary drivers of local adaptation and ecological speciation. By describing how ecological speciation likely occurs more readily at high latitudes, with such nascent species especially prone to extinction by fusion, we derive the ephemeral ecological speciation hypothesis as an integrative mechanistic explanation for latitudinal gradients in species turnover and the net accumulation of biodiversity.