BackgroundThe evolutionary mechanisms involved in shaping complex gene regulatory networks (GRN) that encode for morphologically similar structures in distantly related animals remain elusive. In this context, echinoderm larval skeletons found in brittle stars and sea urchins provide an ideal system. Here, we characterize for the first time the development of the larval skeleton in the ophiuroid Amphiura filiformis and compare it systematically with its counterpart in sea urchin.ResultsWe show that ophiuroids and euechinoids, that split at least 480 Million years ago (Mya), have remarkable similarities in tempo and mode of skeletal development. Despite morphological and ontological similarities, our high-resolution study of the dynamics of genetic regulatory states in A. filiformis highlights numerous differences in the architecture of their underlying GRNs. Importantly, the A.filiformispplx, the closest gene to the sea urchin double negative gate (DNG) repressor pmar1, fails to drive the skeletogenic program in sea urchin, showing important evolutionary differences in protein function. hesC, the second repressor of the DNG, is co-expressed with most of the genes that are repressed in sea urchin, indicating the absence of direct repression of tbr, ets1/2, and delta in A. filiformis. Furthermore, the absence of expression in later stages of brittle star skeleton development of key regulatory genes, such as foxb and dri, shows significantly different regulatory states.ConclusionOur data fill up an important gap in the picture of larval mesoderm in echinoderms and allows us to explore the evolutionary implications relative to the recently established phylogeny of echinoderm classes. In light of recent studies on other echinoderms, our data highlight a high evolutionary plasticity of the same nodes throughout evolution of echinoderm skeletogenesis. Finally, gene duplication, protein function diversification, and cis-regulatory element evolution all contributed to shape the regulatory program for larval skeletogenesis in different branches of echinoderms.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0039-x) contains supplementary material, which is available to authorized users.

Theory predicts that sexual reproduction can increase population viability relative to asexual reproduction by allowing sexual selection in males to remove deleterious mutations from the population without large demographic costs. This requires that selection acts more strongly in males than females and that mutations affecting male reproductive success have pleiotropic effects on population productivity, but empirical support for these assumptions is mixed. We used the seed beetle Callosobruchus maculatus to implement a three‐generation breeding design where we induced mutations via ionizing radiation (IR) in the F0 generation and measured mutational effects (relative to nonirradiated controls) on an estimate of population productivity in the F1 and effects on sex‐specific competitive lifetime reproductive success (LRS) in the F2. Regardless of whether mutations were induced via F0 males or females, they had strong negative effects on male LRS, but a nonsignificant influence on female LRS, suggesting that selection is more efficient in removing deleterious alleles in males. Moreover, mutations had seemingly shared effects on population productivity and competitive LRS in both sexes. Thus, our results lend support to the hypothesis that strong sexual selection on males can act to remove the mutation load on population viability, thereby offering a benefit to sexual reproduction.

Mutation has a fundamental influence over evolutionary processes, but how evolutionary processes shape mutation rate remains less clear. In asexual unicellular organism, increased mutation rates have been observed in stressful environments and the reigning paradigm ascribes this increase to selection for evolvability. However, this explanation does not apply in sexually reproducing species, where little is known about how the environment affects mutation rate. Here we challenged experimental lines of seed beetle, evolved at ancestral temperature or under simulated climate warming, to repair induced mutations at ancestral and stressful temperature. Results show that temperature stress causes individuals to pass on a greater mutation load to their grand-offspring. This suggests that stress-induced mutation rates, in unicellular and multicellular organisms alike, can result from compromised germline DNA repair in low condition individuals. Moreover, lines adapted to simulated climate warming had evolved increased longevity at the cost of reproduction, and this allocation decision improved germline repair. These results suggest that mutation rates can be modulated by resource allocation trade-offs encompassing life-history traits and the germline and have important implications for rates of adaptation and extinction as well as our understanding of genetic diversity in multicellular organisms.

Adaptation in new environments depends on the amount and type of genetic variation available for evolution, and the efficacy by which natural selection discriminates among this variation to favour the survival of the fittest. However, whether some environments systematically reveal more genetic variation in fitness, or impose stronger selection pressures than others, is typically not known. Here, we apply enzyme kinetic theory to show that rising global temperatures are predicted to intensify natural selection systematically throughout the genome by increasing the effects of DNA sequence variation on protein stability. We tested this prediction by i) estimating temperature-dependent fitness effects of induced random mutations in seed beetles adapted to ancestral or warm temperature, and ii) calculating 100 paired selection estimates on mutations in benign versus stressful environments from a diverse set of unicellular and multicellular organisms. Environmental stress per se did not increase the mean strength of selection on de novo mutation, suggesting that the cost of adaptation does not generally increase in new environments to which the organism is maladapted. However, elevated temperature increased the mean strength of selection on genome-wide polymorphism, signified by increases in both mutation load and mutational variance at elevated temperature. The theoretical predictions and empirical data suggest that this increase may correspond to a doubling of genome-wide selection for a predicted 2-4°C climate warming scenario in ectothermic organism living at temperatures close to their thermal optimum. These results have important implications for global patterns of genetic diversity and the rate and repeatability of evolution under climate change.Impact StatementNatural environments are constantly changing so organisms must also change to persist. Whether they can do so ultimately depends upon the reservoir of raw genetic material available for evolution, and the efficacy by which natural selection discriminates among this variation to favour the survival of the fittest. Here, the biochemical properties of molecules and proteins that underpin the link between genotype and phenotype can exert a major influence over how the physical environment affects the expression of phenotypes and the fitness consequences of DNA sequence polymorphism. Yet, the constraints set by these molecular features are often neglected within eco-evolutionary theory trying to predict evolution in new environments. Here we combine predictions from existing biophysical models of protein folding and enzyme kinetics with experimental data from ectothermic organisms across the tree of life, to show that rising global temperatures are predicted to increase the mean strength of selection on DNA sequence variation in cold-blooded organisms. We also show that environmental stress per se generally does not increase the mean strength of selection on new mutations, suggesting that genome-wide natural selection is not stronger in new environments to which an organism is maladapted. Theoretical predictions and data suggest that an expected climate warming scenario of a 2-4°C temperature raise within the forthcoming century will result in roughly a doubling of genome-wide selection for organisms living close to their thermal optima. However, our results also point to substantial variability in the temperature-dependence of selection on different proteins within and between organisms, suggesting scope for compensatory adaptation to shape this relationship. These results bear witness to and extend the universal temperature dependence of biological rates and have important implications for global patterns of genetic diversity and the rate and repeatability of genome evolution under environmental change.