Aligning functional network constraint to evolutionary outcomes

Background. Functional constraint through genomic architecture is suggested to be an important dimension of genome evolution, but quantitative evidence for this idea is rare. In this contribution, existing evidence and discussions on genomic architecture as constraint for convergent evolution, rapid adaptation, and genic adaptation are summarized into alternative, testable hypotheses. Network architecture statistics from protein-protein interaction networks are then used to calculate differences in evolutionary outcomes on the example of genomic evolution among yeast, and the results are used to evaluate statistical support for these longstanding hypotheses. Results.A discriminant function analysis lent statistical support to classifying the yeast interactome into hub, intermediate and peripheral nodes based on network neighborhood connectivity, betweenness centrality, and average shortest path length. Quantitative support for the existence of genomic architecture as mechanistic basis for evolutionary constraint is then revealed through utilizing these statistical parameters of the protein-protein interaction network in combination with estimators of protein evolution. Conclusions.As functional genetic networks are becoming increasingly available, it will now be possible to evaluate functional genetic network constraint against variables describing complex phenotypes and environments, for better understanding of commonly observed deterministic patterns of evolution in non-model organisms. The hypothesis framework and methodological approach outlined herein may help to quantify the extrinsic versus intrinsic dimensions of evolutionary constraint, and result in a better understanding of how fast, effectively, or deterministically organisms adapt

Evidence for an intrinsic factor promoting landscape genetic divergence in Madagascan leaf-litter frogs

The endemic Malagasy frog radiations are an ideal model system to study patterns and processes of speciation in amphibians. Large-scale diversity patterns of these frogs, together with other endemic animal radiations, led to the postulation of new and the application of known hypotheses of species diversification causing diversity patterns in this biodiversity hotspot. Both extrinsic and intrinsic factors have been studied in a comparative framework, with extrinsic factors usually being related to the physical environment (landscape, climate, river catchments, mountain chains), and intrinsic factors being clade-specific traits or constraints (reproduction, ecology, morphology, physiology). Despite some general patterns emerging from such large-scale comparative analyses, it became clear that the mechanism of diversification in Madagascar may vary among clades, and may be a multifactorial process. In this contribution, I test for intrinsic factors promoting population-level divergence within a clade of terrestrial, diurnal leaf-litter frogs (genus Gephyromantis) that has previously been shown to diversify according to extrinsic factors. Landscape genetic analyses of the microendemic species Gephyromantis enki and its widely distributed, larger sister species Gephyromantis boulengeri over a rugged landscape in the Ranomafana area shows that genetic variance of the smaller species cannot be explained by landscape resistance alone. Both topographic and riverine barriers are found to be important in generating this divergence. This case study yields additional evidence for the probable importance of body size in lineage diversification

Ecomorphological Variation in Three Species of Cybotoid Anoles

© 2018 by The Herpetologists' League, Inc. Caribbean Anolis lizards exhibit a complex suite of ecological, morphological, and behavioral traits that allow their specialization to particular microhabitats. These microhabitat specialists, called ecomorphs, have independently evolved on the four islands of the Greater Antilles, and diversification among anole ecomorphs has been the focus of many studies. Yet, habitat specialization has also occurred among species within the same ecomorph group. Here, we examined ecological, morphological, and behavioral divergence in three Hispaniolan trunk-ground species, the cybotoid anoles: Anolis cybotes, A. marcanoi, and A. longitibialis. We found differences in limb morphology, locomotor behavior, and perch use among the three cybotoid species that mirror differences across the ecomorphs. Among these species of cybotoids, those that have longer limbs tend to move less frequently, occupy broader perches, and have smaller fourth toes with fewer lamellae. We also observed that the species with greater male-biased size dimorphism had larger heads, smaller dewlaps, and smaller testes. These results are consistent with the predictions of sexual selection theory, in that species with large male body size may have larger heads because of increased male-male combat, and smaller testes potentially attributable to a trade-off between pre- and postcopulatory selection. Overall, our study suggests that a combination of local adaptation to different structural habitats and sexual selection might produce ecomorphological diversification within cybotoid anoles of the same ecomorph group

Genomic and phenotypic signatures of climate adaptation in an Anolis lizard

Integrated knowledge on phenotype, physiology and genomic adaptations is required to understand the effects of climate on evolution. The functional genomic basis of organismal adaptation to changes in the abiotic environment, its phenotypic consequences, and its possible convergence across vertebrates, are still understudied. In this study, we use a comparative approach to verify predicted gene functions for vertebrate thermal adaptation with observed functions underlying repeated genomic adaptations in response to elevation in the lizard Anolis cybotes. We establish a direct link between recurrently evolved phenotypes and functional genomics of altitude-related climate adaptation in three highland and lowland populations in the Dominican Republic. We show that across vertebrates, genes contained in this interactome are expressed within the brain and during development. These results are relevant to elucidate the effect of global climate change across vertebrates, and might aid in furthering insight into gene-environment relationships under disturbances to external homeostasis

Plant phenology supports the multi-emergence hypothesis for ebola spillover events

Ebola virus disease outbreaks in animals (including humans and great apes) start with sporadic host switches from unknown reservoir species. The factors leading to such spillover events are little explored. Filoviridae viruses have a wide range of natural hosts and are unstable once outside hosts. Spillover events, which involve the physical transfer of viral particles across species, could therefore be directly promoted by conditions of host ecology and environment. In this report we outline a proof of concept that temporal fluctuations of a set of ecological and environmental variables describing the dynamics of the host ecosystem are able to predict such events of Ebola virus spillover to humans and animals. We compiled a dataset of climate and plant phenology variables and Ebola virus disease spillovers in humans and animals. We identified critical biotic and abiotic conditions for spillovers via multiple regression and neural networks based time series regression. Phenology variables proved to be overall better predictors than climate variables. African phenology variables are not yet available as a comprehensive online resource. Given the likely importance of phenology for forecasting the likelihood of future Ebola spillover events, our results highlight the need for cost-effective transect surveys to supply phenology data for predictive modelling efforts

Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases

Wollenberg Valero KC, Garcia-Porta J, Rodriguez A, et al. Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases. Nature Communications. 2017;8(1): 15213.Anuran amphibians undergo major morphological transitions during development, but the contribution of their markedly different life-history phases to macroevolution has rarely been analysed. Here we generate testable predictions for coupling versus uncoupling of phenotypic evolution of tadpole and adult life-history phases, and for the underlying expression of genes related to morphological feature formation. We test these predictions by combining evidence from gene expression in two distantly related frogs, Xenopus laevis and Mantidactylus betsi-leanus, with patterns of morphological evolution in the entire radiation of Madagascan mantellid frogs. Genes linked to morphological structure formation are expressed in a highly phase-specific pattern, suggesting uncoupling of phenotypic evolution across life-history phases. This gene expression pattern agrees with uncoupled rates of trait evolution among life-history phases in the mantellids, which we show to have undergone an adaptive radiation. Our results validate a prevalence of uncoupling in the evolution of tadpole and adult phenotypes of frogs

A candidate multimodal functional genetic network for thermal adaptation

Vertebrate ectotherms such as reptiles provide ideal organisms for the study of adaptation to environmental thermal change. Comparative genomic and exomic studies can recover markers that diverge between warm and cold adapted lineages, but the genes that are functionally related to thermal adaptation may be difficult to identify. We here used a bioinformatics genome-mining approach to predict and identify functions for suitable candidate markers for thermal adaptation in the chicken. We first established a framework of candidate functions for such markers, and then compiled the literature on genes known to adapt to the thermal environment in different lineages of vertebrates. We then identified them in the genomes of human, chicken, and the lizard Anolis carolinensis, and established a functional genetic interaction network in the chicken. Surprisingly, markers initially identified from diverse lineages of vertebrates such as human and fish were all in close functional relationship with each other and more associated than expected by chance. This indicates that the general genetic functional network for thermoregulation and/or thermal adaptation to the environment might be regulated via similar evolutionarily conserved pathways in different vertebrate lineages. We were able to identify seven functions that were statistically overrepresented in this network, corresponding to four of our originally predicted functions plus three unpredicted functions. We describe this network as multimodal: central regulator genes with the function of relaying thermal signal (1), affect genes with different cellular functions, namely (2) lipoprotein metabolism, (3) membrane channels, (4) stress response, (5) response to oxidative stress, (6) muscle contraction and relaxation, and (7) vasodilation, vasoconstriction and regulation of blood pressure. This network constitutes a novel resource for the study of thermal adaptation in the closely related nonavian reptiles and other vertebrate ectotherms

Transcriptomic signatures of experimental alkaloid consumption in a poison frog

© 2019 by the authors. Licensee MDPI, Basel, Switzerland. In the anuran family Dendrobatidae, aposematic species obtain their toxic or unpalatable alkaloids from dietary sources, a process known as sequestering. To understand how toxicity evolved in this family, it is paramount to elucidate the pathways of alkaloid processing (absorption, metabolism, and sequestering). Here, we used an exploratory skin gene expression experiment in which captive-bred dendrobatids were fed alkaloids. Most of these experiments were performed with Dendrobates tinctorius, but some trials were performed with D. auratus, D. leucomelas and Allobates femoralis to explore whether other dendrobatids would show similar patterns of gene expression. We found a consistent pattern of up-regulation of genes related to muscle and mitochondrial processes, probably due to the lack of mutations related to alkaloid resistance in these species. Considering conserved pathways of drug metabolism in vertebrates, we hypothesize alkaloid degradation is a physiological mechanism of resistance, which was evidenced by a strong upregulation of the immune system in D. tinctorius, and of complement C2 across the four species sampled. Probably related to this strong immune response, we found several skin keratins downregulated, which might be linked to a reduction of the cornified layer of the epidermis. Although not conclusive, our results offer candidate genes and testable hypotheses to elucidate alkaloid processing in poison frogs

Functional genomics of abiotic environmental adaptation in lacertid lizards and other vertebrates

Understanding the genomic basis of adaptation to different abiotic environments is important in the context of climate change and resulting short-term environmental fluctuations. Using functional and comparative genomics approaches, we here investigated whether signatures of genomic adaptation to a set of environmental parameters are concentrated in specific subsets of genes and functions in lacertid lizards and other vertebrates. We first identify 200 genes with signatures of positive diversifying selection from transcriptomes of 24 species of lacertid lizards and demonstrate their involvement in physiological and morphological adaptations to climate. To understand how functionally similar these genes are to previously predicted candidate functions for climate adaptation and to compare them with other vertebrate species, we then performed a meta-analysis of 1,100 genes under selection obtained from -omics studies in vertebrate species adapted to different abiotic factors. We found that the vertebrate gene set formed a tightly connected interactome, which was to 23% enriched in previously predicted functions of adaptation to climate, and to a large part (18%) involved in organismal stress response. We found a much higher degree of identical genes being repeatedly selected among different animal groups (43.6%), and of functional similarity and post-translational modifications than expected by chance, and no clear functional division between genes used for ectotherm and endotherm physiological strategies. In total, 171 out of 200 genes of Lacertidae were part of this network. These results highlight an important role of a comparatively small set of genes and their functions in environmental adaptation and narrow the set of candidate pathways and markers to be used in future research on adaptation and stress response related to climate change

An endless harvest: integrative revision of the Gephyromantis boulengeri and G. blanci complexes reveals six new species of mantellid frogs from Madagascar

The Malagasy genus Gephyromantis contains 51 species of primarily terrestrial or scansorial frogs. Although many species are morphologically weakly divergent from each other, the combination of molecular and bioacoustic evidence has led to a continuous flow of species discoveries in the last years. Previous works have notably shown the existence of numerous additional deep mitochondrial lineages of uncertain status in the nominal subgenus Gephyromantis, some of these considered as confirmed or unconfirmed candidate species, some as deep conspecific lineages. Here we use DNA sequences of one mitochondrial and one nuclear marker, as well as morphological and bioacoustic data, to conduct an integrative revision of the subgenus Gephyromantis. The analyses reveal at least 12 distinct and independent evolutionary lineages belonging to the G. blanci and G. boulengeri species complexes. Evidence for the species status of these lineages included multiple cases of syntopic occurrence without genetic admixture, as well as differences in advertisement calls or morphological differentiation without intermediate forms, suggesting reproductive isolation. We discuss the relevance of these different lines of evidence and describe six new species of Gephyromantis.The work of AM was supported by the Deutsche Forschungsgemeinschaft (grant MI 2748/1-1) and the work of AC was supported by the Portuguese National Funds through FCT (Fundação para a Ciência e a Tecnologia, contract 2020.00823. CEECIND/CP1601/CT0003).Peer reviewe