Adaptive Optima Research Articles

Multidimensional primate niche space sheds light on interspecific competition in primate evolution

Characterising how the totality of primate diversity is distributed across the order, and how it evolved, is challenging because diversity in individual traits often show opposing phylogenetic patterns. A species’ combination of traits can be conceptualised as its ‘niche’. Here, we describe and analyse seven-dimensional niche space, comprising 11 traits, for 191 primate species. Multifaceted diversity is distributed unequally among taxonomic groups. Cercopithecoidea and Hominidae occupy the largest areas of niche space, and are the most diverse families; platyrrhine families occupy small areas, and this space overlaps with strepsirrhines. The evolution of species’ locations in niche space is regulated by selection for adaptive optima in trait combinations. Given that niche similarity results in interspecific competition, we quantify two measures of species’ niche locations relative to others. We find that omnivores, frugivores, and species tolerating higher temperatures experience stronger interspecific competition. Hominidae occupation of niche space suggests competitive exclusion from niches by Cercopithecoidea over evolutionary time; but living great apes experience the lowest levels of interspecific competition. Callitrichids experience the highest levels of interspecific competition. Our results provide a standardised measure of primate niches that sheds light on the partitioning and evolution of primate diversity, and how this is driven by interspecific competition.

Color morphs of the fire salamander are discriminated at night by conspecifics and predators

AbstractThe coexistence of multiple discrete color phenotypes (i.e. color polymorphism) has been studied in many diurnal species where environmental light allows most visual systems to chromatically discriminate color morphs. However, there is a large gap in our understanding of the discrimination thresholds and the function color polymorphisms play at night. We collected spectral data from the throats of red‐ and yellow‐morph males in a polymorphic population of the nocturnal amphibian Salamandra salamandra gallaica. We estimated the discriminability between morphs and their conspicuousness at night by fitting visual models of conspecifics and predators. We also collected morphological, behavioral and physiological data and assessed the abundance and activity patterns of each morph to explore their potential function. Visual models indicated that both conspecifics and predators can visually discriminate salamander color morphs under night‐light conditions. Assuming the potential role of yellow and red color patches as visual signals, putatively related to social signaling, we could suspect that these colors represent different adaptive optima. Red‐morph individuals had shorter bodies and lower body condition, but both morphs showed similar space use. In addition, both color morphs exhibited similar metabolic physiology, suggesting that the observed similarity in these traits may be better explained by the shared environmental conditions, rather than color. Finally, differences in the conspicuousness of red and yellow morphs could result in differential predation pressure.

Diadromy Drives Elevated Rates of Trait Evolution and Ecomorphological Convergence in Clupeiformes (Herring, Shad, and Anchovies).

AbstractMigration can have a profound influence on rates and patterns of phenotypic evolution. Diadromy is the migration between marine and freshwater habitats for feeding and reproduction that can require individuals to travel tens to thousands of kilometers. The high energetic demands of diadromy are predicted to select for ecomorphological traits that maximize swimming and locomotor efficiency. Intraspecific studies have shown repeated instances of divergence among diadromous and nondiadromous populations in locomotor and foraging traits, which suggests that at a macroevolutionary scale diadromous lineages may experience convergent evolution onto one or multiple adaptive optima. We tested for differences in rates and patterns of phenotypic evolution among diadromous and nondiadromous lineages in Clupeiformes, a clade that has evolved diadromy more than 10 times. Our results show that diadromous clupeiforms show convergent evolution for some locomotor traits and faster rates of evolution, which we propose are adaptive responses to the locomotor demands of migration. We also find evidence that diadromous lineages show convergence into multiple regions of multivariate trait space and suggest that these respective trait spaces are associated with differences in migration and trophic ecology. However, not all locomotor traits and no trophic traits show evidence of convergence or elevated rates of evolution associated with diadromy. Our results show that long-distance migration influences the tempo and patterns of phenotypic evolution at macroevolutionary scales, but there is not a single diadromous syndrome.

Using landscape genomics to delineate future adaptive potential for climate change in the Yosemite toad (Anaxyrus canorus).

An essential goal in conservation biology is delineating population units that maximize the probability of species persisting into the future and adapting to future environmental change. However, future-facing conservation concerns are often addressed using retrospective patterns that could be irrelevant. We recommend a novel landscape genomics framework for delineating future "Geminate Evolutionary Units" (GEUs) in a focal species: (1) identify loci under environmental selection, (2) model and map adaptive conservation units that may spawn future lineages, (3) forecast relative selection pressures on each future lineage, and (4) estimate their fitness and likelihood of persistence using geo-genomic simulations. Using this process, we delineated conservation units for the Yosemite toad (Anaxyrus canorus), a U.S. federally threatened species that is highly vulnerable to climate change. We used a genome-wide dataset, redundancy analysis, and Bayesian association methods to identify 24 candidate loci responding to climatic selection (R 2 ranging from 0.09 to 0.52), after controlling for demographic structure. Candidate loci included genes such as MAP3K5, involved in cellular response to environmental change. We then forecasted future genomic response to climate change using the multivariate machine learning algorithm Gradient Forests. Based on all available evidence, we found three GEUs in Yosemite National Park, reflecting contrasting adaptive optima: YF-North (high winter snowpack with moderate summer rainfall), YF-East (low to moderate snowpack with high summer rainfall), and YF-Low-Elevation (low snowpack and rainfall). Simulations under the RCP 8.5 climate change scenario suggest that the species will decline by 29% over 90 years, but the highly diverse YF-East lineage will be least impacted for two reasons: (1) geographically it will be sheltered from the largest climatic selection pressures, and (2) its standing genetic diversity will promote a faster adaptive response. Our approach provides a comprehensive strategy for protecting imperiled non-model species with genomic data alone and has wide applicability to other declining species.

Ontogenetic drivers of morphological evolution in monitor lizards and allies (Squamata: Paleoanguimorpha), a clade with extreme body size disparity

BackgroundHeterochrony, change in the rate or timing of development, is thought to be one of the main drivers of morphological evolution, and allometry, trait scaling patterns imposed by size, is traditionally thought to represent an evolutionary constraint. However, recent studies suggest that the ontogenetic allometric trajectories describing how organisms change as they grow may be labile and adaptive. Here we investigated the role of postnatal ontogenetic development in the morphological diversification of Paleoanguimorpha, the monitor lizards and allies, a clade with extreme body size disparity. We obtained linear and geometric morphometric data for more than 1,600 specimens belonging to three families and 60 species, representing ~ 72% of extant paleoanguimorph diversity. We used these data to undertake one of the largest comparative studies of ontogenetic allometry to date.ResultsHeterochrony is likely dictating morphological divergence at shallow evolutionary scales, while changes in the magnitude and direction of ontogenetic change are found mainly between major clades. Some patterns of ontogenetic variation and morphological disparity appear to reflect ontogenetic transitions in habitat use. Generally, juveniles are more similar to each other than adults, possibly because species that differ in ecology as adults are arboreal as juveniles. The magnitude of ontogenetic change follows evolutionary models where variation is constrained around an optimal value. Conversely, the direction of ontogenetic change may follow models with different adaptive optima per habitat use category or models where interspecific interactions influence its evolution. Finally, we found that the evolutionary rates of the ontogenetic allometric trajectories are phylogenetically variable.ConclusionsThe attributes of ontogenetic allometric trajectories and their evolutionary rates are phylogenetically heterogeneous in Paleoanguimorpha. Both allometric constraints and ecological factors have shaped ontogeny in the group. Our study highlights the evolutionary lability and adaptability of postnatal ontogeny, and teases apart how different evolutionary shifts in ontogeny contribute to the generation of morphological diversity at different evolutionary scales.

You are more than what you eat: potentially adaptive enrichment of microbiome functions across bat dietary niches.

BackgroundAnimals evolved in a microbial world, and their gut microbial symbionts have played a role in their ecological diversification. While many recent studies report patterns of phylosymbiosis between hosts and their gut bacteria, fewer studies examine the potentially adaptive functional contributions of these microbes to the dietary habits of their hosts. In this study, we examined predicted metabolic pathways in the gut bacteria of more than 500 individual bats belonging to 60 species and compare the enrichment of these functions across hosts with distinct dietary ecologies.ResultsWe found that predicted microbiome functions were differentially enriched across hosts with different diets. Using a machine-learning approach, we also found that inferred microbiome functions could be used to predict specialized host diets with reasonable accuracy. We detected a relationship between both host phylogeny and diet with respect to microbiome functional repertoires. Because many predicted functions could potentially fill nutritional gaps for bats with specialized diets, we considered pathways discriminating dietary niches as traits of the host and fit them to comparative phylogenetic models of evolution. Our results suggest that some, but not all, predicted microbiome functions may evolve toward adaptive optima and thus be visible to the forces of natural selection operating on hosts over evolutionary time.ConclusionsOur results suggest that bats with specialized diets may partially rely on their gut microbes to fulfill or augment critical nutritional pathways, including essential amino acid synthesis, fatty acid biosynthesis, and the generation of cofactors and vitamins essential for proper nutrition. Our work adds to a growing body of literature suggesting that animal microbiomes are structured by a combination of ecological and evolutionary processes and sets the stage for future metagenomic and metabolic characterization of the bat microbiome to explore links between bacterial metabolism and host nutrition.

Phylogeographical analysis of character displacement in feeding phenotypes of snail-feedingAcoptolabrusground beetles

AbstractEcological character displacement predicts that interspecific resource competition results in greater trait divergence between species in sympatry than in allopatry. However, other processes, such as ecological sorting, result in the same pattern of trait variation. In this study, we characterize character displacement in eight species of snail-feeding Acoptolabrus ground beetles in the Far East. Acoptolabrus exhibit divergent feeding phenotypes, including species with a slender forebody that is able to intrude into large shells and species with stout heads and mandibles for crushing small shells. The pattern of character displacement in feeding phenotypes was confirmed by multivariate analysis of body dimensions. Molecular phylogenetic analysis, divergence time estimation and biogeographical analysis revealed that sympatry and phenotypic divergence occurred repeatedly during the Pleistocene and almost simultaneously within each geographical area. Comparative analysis revealed that the evolution of feeding phenotypes best fitted a selective model with three adaptive optima, corresponding to the three cases of sympatry with a congener. Repeated coincidences of sympatry and adaptive differentiation in feeding phenotypes suggested causal relationships, although the precise order of events was difficult to discriminate. This study provides insight into the spatiotemporal dynamics of interspecific interactions and adaptive phenotypic diversification.

Feeding specialization and longer generation time are associated with relatively larger brains in bees

Despite their miniature brains, insects exhibit substantial variation in brain size. Although the functional significance of this variation is increasingly recognized, research on whether differences in insect brain sizes are mainly the result of constraints or selective pressures has hardly been performed. Here, we address this gap by combining prospective and retrospective phylogenetic-based analyses of brain size for a major insect group, bees (superfamily Apoidea). Using a brain dataset of 93 species from North America and Europe, we found that body size was the single best predictor of brain size in bees. However, the analyses also revealed that substantial variation in brain size remained even when adjusting for body size. We consequently asked whether such variation in relative brain size might be explained by adaptive hypotheses. We found that ecologically specialized species with single generations have larger brains-relative to their body size-than generalist or multi-generation species, but we did not find an effect of sociality on relative brain size. Phylogenetic reconstruction further supported the existence of different adaptive optima for relative brain size in lineages differing in feeding specialization and reproductive strategy. Our findings shed new light on the evolution of the insect brain, highlighting the importance of ecological pressures over social factors and suggesting that these pressures are different from those previously found to influence brain evolution in other taxa.

Phylogenomics, Biogeography, and Morphometrics Reveal Rapid Phenotypic Evolution in Pythons After Crossing Wallace's Line.

Ecological opportunities can be provided to organisms that cross stringent biogeographic barriers towards environments with new ecological niches. Wallace's and Lyddeker's lines are arguably the most famous biogeographic barriers, separating the Asian and Australo-Papuan biotas. One of the most ecomorphologically diverse groups of reptiles, the pythons, is distributed across these lines, and are remarkably more diverse in phenotype and ecology east of Lydekker's line in Australo-Papua. We used an anchored hybrid enrichment approach, with near complete taxon sampling, to extract mitochondrial genomes and 376 nuclear loci to resolve and date their phylogenetic history. Biogeographic reconstruction demonstrates that they originated in Asia around 38-45 Ma and then invaded Australo-Papua around 23 Ma. Australo-Papuan pythons display a sizeable expansion in morphological space, with shifts towards numerous new adaptive optima in head and body shape, coupled with the evolution of new micro-habitat preferences. We provide an updated taxonomy of pythons and our study also demonstrates how ecological opportunity following colonization of novel environments can promote morphological diversification in a formerly ecomorphologically conservative group. [Adaptive radiation; anchored hybrid enrichment; biogeography; morphometrics; snakes.].

Toxin expression in snake venom evolves rapidly with constant shifts in evolutionary rates.

Key innovations provide ecological opportunity by enabling access to new resources, colonization of new environments, and are associated with adaptive radiation. The most well-known pattern associated with adaptive radiation is an early burst of phenotypic diversification. Venoms facilitate prey capture and are widely believed to be key innovations leading to adaptive radiation. However, few studies have estimated their evolutionary rate dynamics. Here, we test for patterns of adaptive evolution in venom gene expression data from 52 venomous snake species. By identifying shifts in tempo and mode of evolution along with models of phenotypic evolution, we show that snake venom exhibits the macroevolutionary dynamics expected of key innovations. Namely, all toxin families undergo shifts in their rates of evolution, likely in response to changes in adaptive optima. Furthermore, we show that rapid-pulsed evolution modelled as a Lévy process better fits snake venom evolution than conventional early burst or Ornstein–Uhlenbeck models. While our results support the idea of snake venom being a key innovation, the innovation of venom chemistry lacks clear mechanisms that would lead to reproductive isolation and thus adaptive radiation. Therefore, the extent to which venom directly influences the diversification process is still a matter of contention.

Experimental Evidence That Metamorphosis Alleviates Genomic Conflict.

Whenever genetically correlated traits experience antagonistic selection, an adaptive response in one trait can lead to a maladaptive response in the correlated trait. This is a form of genome-level conflict that can have important evolutionary consequences by impeding organisms from reaching their adaptive optima. Antagonistic selection should be pervasive in organisms with complex life histories because larval and adult life stages specialize in dramatically different environments. Since individuals express larval and adult morphologies from a single genome, genomic conflict across ontogenetic stages should also be prevalent. Using wood frogs as a study system, we measured natural selection on larval and postmetamorphic life stages and estimated genetic correlations among traits. Alternative life stages experienced a mix of both antagonistic and congruent viability selection. The integration between traits changed over the course of metamorphosis, reducing genetic correlations that cause conflict. Our results provide novel experimental evidence that metamorphosis can alleviate genomic conflict by partitioning life-history stages into modules that can more readily respond to selection. These results highlight the adaptive potential of metamorphosis as a means to avoid ecological specialization trade-offs. Moreover, they provide insights into the prevalence and evolutionary maintenance of complex life cycles.

Divergence, Convergence and Phenotypic Diversity of Neotropical Frugivorous Bats

Knowing how adaptation shapes morphological evolution is fundamental to understanding the processes that promote biological diversity. However, there is a lack of empirical evidence on the effects of adaptive radiations on phenotypic diversity, which is related to processes that promote phenotypic divergence and convergence. We applied comparative methods to identify shifts in adaptive peaks and to detect divergence and convergence in skull morphology of frugivorous bats (Phyllostomidae: Stenodermatinae and Carollinae), an ecologically diverse group with strong association between skull morphology, feeding performance and diet that suggests adaptive diversification through morphological innovation. We found divergence and convergence for skull morphology. Fifteen peak shifts were found for jaws, which result in four convergent and four divergent regimes. For skull, nine peak shifts were detected that result in three convergent and three divergent regimes. Furthermore, convergence was significant and strong for skull morphology since distantly related organisms converged to the same adaptive optima. Results suggest that convergence indicates the effect of restriction on phenotypes to keep the advantages provided by the skull phenotype that played a central role in the evolution of strict frugivory in phyllostomids. We conclude that convergence has limited phenotypic diversity of functional traits related to feeding in phyllostomid frugivores.

Phylogenetic patterns of trait and trait plasticity evolution: Insights from amphibian embryos.

Environmental variation favors the evolution of phenotypic plasticity. For many species, we understand the costs and benefits of different phenotypes, but we lack a broad understanding of how plastic traits evolve across large clades. Using identical experiments conducted across North America, we examined prey responses to predator cues. We quantified five life-history traits and the magnitude of their plasticity for 23 amphibian species/populations (spanning three families and five genera) when exposed to no cues, crushed-egg cues, and predatory crayfish cues. Embryonic responses varied considerably among species and phylogenetic signal was common among the traits, whereas phylogenetic signal was rare for trait plasticities. Among trait-evolution models, the Ornstein-Uhlenbeck (OU) model provided the best fit or was essentially tied with Brownian motion. Using the best fitting model, evolutionary rates for plasticities were higher than traits for three life-history traits and lower for two. These data suggest that the evolution of life-history traits in amphibian embryos is more constrained by a species' position in the phylogeny than is the evolution of life history plasticities. The fact that an OU model of trait evolution was often a good fit to patterns of trait variation may indicate adaptive optima for traits and their plasticities.

Morph-specific assortative mating in common wall lizard females.

Color polymorphism often is associated with alternative reproductive strategies and may reflect different adaptive optima that coexist within populations. The equilibrium among morph frequencies is maintained by the occurrence of opposite selective pressures (disruptive vs. stabilizing), which promote polymorphism while preserving gene flow. Sexual selection may contribute on both sides, particularly when morphs do not mate randomly. Reptiles offer a good model, notably lizards. Nevertheless, previous studies on mate choice in polymorphic lizards have generated contrasting results, with some studies suggesting that female morphs might tune their preference depending on environmental/social conditions such as crowding. We experimentally manipulated the number of individuals a female common wall lizard Podarcis muralis perceives around her, to test if females of different morphs (white or yellow) tune their choice for white and yellow males in order to maximize the probability that hatchlings follow the strategy best adapted to the population density. Results showed that crowding experienced by females did not affect mate choice, arguing against a flexible choice strategy by females. However, white females significantly associated with white males, whereas yellow females did not significantly associate with yellow males. Thus, sexual selection could contribute to the maintenance of color polymorphism in this species by a mix of assortative and non-assortative mating strategies, which could maintain the equilibrium between gene divergence and gene flow among morphs.

Performance Tradeoffs, Ontogenetic Conflict, and Multisport Athletes: How is an Ironman Triathlete Like a Frog?

Life-history theory is a cornerstone of modern evolutionary biology that addresses myriad phenomena ranging from demography and population structure to the evolution of aging and senescence. Trade-offs may arise in a number of contexts, from allocation-based (e.g., egg size vs. egg number) to genomic conflicts (e.g., intralocus sexual conflict in which genes that perform well in males perform poorly in females). Here we test for performance tradeoffs in human athletes. We show that in Ironman triathletes, swimming performance trades off with cycling and running performance. The tradeoff appears to be plastic, in that only highly trained athletes experience the tradeoff. We then investigate whether wood frogs (Rana sylvatica) experience similar locomotor performance tradeoffs, to ask whether the divergent environments experienced by tadpoles and frogs leads to ontogenetic conflict (tradeoffs over development). We show that although swimming and jumping performance are positively correlated, antagonistic natural selection may still favor alternative adaptive optima in the two life history stages. However, "adaptive decoupling" of the life stages during metamorphosis may resolve ontogenetic conflict and facilitate independent adaptation to both environments. Thus, whereas performance tradeoffs are general in both systems, the unique selective environment of amphibians has favored the evolution of mechanisms to alleviate the costs of those tradeoffs.

Ecological diversification associated with the benthic‐to‐pelagic transition by North American minnows

Ecological opportunity is often regarded as a key factor that explains why diversity is unevenly distributed across life. Colonization of novel environments or adaptive zones may promote diversification. North American minnows exhibit an ancestral benthic-to-pelagic habitat shift that coincided with a burst in diversification. Here, we evaluate the phenotypic and ecological implications of this habitat shift by assessing craniofacial and dietary traits among 34 species and testing for morphology-diet covariation, convergence and adaptive optima. There were several instances of morphology-diet covariation such as correlations between mouth angle and the consumption of terrestrial insects and between relative gut length and the consumption of algae. After accounting for size and phylogenetic nonindependence, benthic species had longer heads, longer snouts, eyes positioned higher on their head, smaller mouth angles and longer digestive tracts than pelagic minnows. Benthic minnows also consumed more algae but less terrestrial insects, by volume, than pelagic minnows. Lastly, there were three distinct evolutionary regimes and more convergence in morphology and dietary characteristics than expected under a Brownian motion model of evolution. These findings indicate that colonization of the pelagic zone by minnows involved myriad phenotypic and dietary changes associated with exploitation of terrestrial subsidies. Thus, minnows exhibit phenotype-dietary covariation, an expansion of ecological roles and a burst in diversification rates in response to the ecological opportunity afforded by the colonization of a novel habitat.

The dual role of Andean topography in primary divergence: functional and neutral variation among populations of the hummingbird, Metallura tyrianthina.

BackgroundThe ridges and valleys of the Andes create physical barriers that limit animal dispersal and cause deterministic local variation in rainfall. This has resulted in physical isolation of animal populations and variation in habitats, each of which has likely contributed to the evolution of high species diversity in the region. However, the relative influences of geographic isolation, ecoclimatic conditions, and their potential interactions remain poorly understood. To address this, we compared patterns of genetic and morphological diversity in Peruvian populations of the hummingbird Metallura tyrianthina.ResultsPhylogenetic and variation partitioning analyses showed that geographic isolation rather than climatic dissimilarity explained the greatest proportion of genetic variance. In contrast, bill length variation was explained by climatic seasonality, but not by genetic divergence. We found that mutation-scaled migration rate (m) between persistently humid and semi-humid environments was nearly 20 times higher when the habitats were contiguous (m = 39.9) than when separated by a barrier, the Cordillera de Vilcanota (m = 2.1). Moreover, the population experiencing more gene flow exhibited a lesser degree of bill length divergence despite similar differences in climate.ConclusionsGeographic isolation is necessary for genetic divergence. Ecological differences, represented here by climate characteristics, are necessary for functional divergence. Gene flow appears to hinder the evolution of functional traits toward local adaptive optima. This suggests that functional diversification requires geographic isolation followed or accompanied by a shift in ecological conditions. Andean topography causes both isolation and climatic variation, underscoring its dual role in biotic diversification.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0595-2) contains supplementary material, which is available to authorized users.

Modeling the Population-Level Processes of Biodiversity Gain and Loss at Geological Timescales.

The path of species diversification is commonly observed by inspecting the fossil record. Yet, how species diversity changes at geological timescales relate to lower-level processes remains poorly understood. Here we use mathematical models of spatially structured populations to show that natural selection and gradual environmental change give rise to discontinuous phenotype changes that can be connected to speciation and extinction at the macroevolutionary level. In our model, new phenotypes arise in the middle of the environmental gradient, while newly appearing environments are filled by existing phenotypes shifting their adaptive optima. Slow environmental change leads to loss of phenotypes in the middle of the extant environmental range, whereas fast change causes extinction at one extreme of the environmental range. We compared our model predictions against a well-known yet partially unexplained pattern of intense hoofed mammal diversification associated with grassland expansion during the Late Miocene. We additionally used the model outcomes to cast new insight into Cope's law of the unspecialized. Our general finding is that the rate of environmental change determines where generation and loss of diversity occur in the phenotypic and physical spaces.

Selection towards different adaptive optima drove the early diversification of locomotor phenotypes in the radiation of Neotropical geophagine cichlids

BackgroundSimpson envisaged a conceptual model of adaptive radiation in which lineages diversify into “adaptive zones” within a macroevolutionary adaptive landscape. However, only a handful of studies have empirically investigated this adaptive landscape and its consequences for our interpretation of the underlying mechanisms of phenotypic evolution. In fish radiations the evolution of locomotor phenotypes may represent an important dimension of ecomorphological diversification given the implications of locomotion for feeding and habitat use. Neotropical geophagine cichlids represent a newly identified adaptive radiation and provide a useful system for studying patterns of locomotor diversification and the implications of selective constraints on phenotypic divergence in general.ResultsWe use multivariate ordination, models of phenotypic evolution and posterior predictive approaches to investigate the macroevolutionary adaptive landscape and test for evidence of early divergence of locomotor phenotypes in Geophagini. The evolution of locomotor phenotypes was characterized by selection towards at least two distinct adaptive peaks and the early divergence of modern morphological disparity. One adaptive peak included the benthic and epibenthic invertivores and was characterized by fishes with deep, laterally compressed bodies that optimize precise, slow-swimming manoeuvres. The second adaptive peak resulted from a shift in adaptive optima in the species-rich ram-feeding/rheophilic Crenicichla-Teleocichla clade and was characterized by species with streamlined bodies that optimize fast starts and rapid manoeuvres. Evolutionary models and posterior predictive approaches favoured an early shift to a new adaptive peak over decreasing rates of evolution as the underlying process driving the early divergence of locomotor phenotypes.ConclusionsThe influence of multiple adaptive peaks on the divergence of locomotor phenotypes in Geophagini is compatible with the expectations of an ecologically driven adaptive radiation. This study confirms that the diversification of locomotor phenotypes represents an important dimension of phenotypic evolution in the geophagine adaptive radiation. It also suggests that the commonly observed early burst of phenotypic evolution during adaptive radiations may be better explained by the concentration of shifts to new adaptive peaks deep in the phylogeny rather than overall decreasing rates of evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0348-7) contains supplementary material, which is available to authorized users.

Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies.

Understanding the genetic architecture of adaptive traits has been at the centre of modern evolutionary biology since Fisher; however, evaluating how the genetic architecture of ecologically important traits influences their diversification has been hampered by the scarcity of empirical data. Now, high-throughput genomics facilitates the detailed exploration of variation in the genome-to-phenotype map among closely related taxa. Here, we investigate the evolution of wing pattern diversity in Heliconius, a clade of neotropical butterflies that have undergone an adaptive radiation for wing-pattern mimicry and are influenced by distinct selection regimes. Using crosses between natural wing-pattern variants, we used genome-wide restriction site-associated DNA (RAD) genotyping, traditional linkage mapping and multivariate image analysis to study the evolution of the architecture of adaptive variation in two closely related species: Heliconius hecale and H. ismenius. We implemented a new morphometric procedure for the analysis of whole-wing pattern variation, which allows visualising spatial heatmaps of genotype-to-phenotype association for each quantitative trait locus separately. We used the H. melpomene reference genome to fine-map variation for each major wing-patterning region uncovered, evaluated the role of candidate genes and compared genetic architectures across the genus. Our results show that, although the loci responding to mimicry selection are highly conserved between species, their effect size and phenotypic action vary throughout the clade. Multilocus architecture is ancestral and maintained across species under directional selection, whereas the single-locus (supergene) inheritance controlling polymorphism in H. numata appears to have evolved only once. Nevertheless, the conservatism in the wing-patterning toolkit found throughout the genus does not appear to constrain phenotypic evolution towards local adaptive optima.