Recent adaptive radiations are models for investigating mechanisms contributing to the evolution of biodiversity. An unresolved question is the relative importance of new mutations, ancestral variants, and introgressive hybridization for phenotypic evolution and speciation. Here, we address this issue using Darwin’s finches and investigate the genomic architecture underlying their phenotypic diversity. Admixture mapping for beak and body size in the small, medium, and large ground finches revealed 28 loci showing strong genetic differentiation. These loci represent ancestral haplotype blocks with origins predating speciation events during the Darwin’s finch radiation. Genes expressed in the developing beak are overrepresented in these genomic regions. Ancestral haplotypes constitute genetic modules for selection and act as key determinants of the unusual phenotypic diversity of Darwin’s finches. Such ancestral haplotype blocks can be critical for how species adapt to environmental variability and change.

/pdf/rapid-adaptive-radiation-of-darwins-finches-depends-on-36slb0hu.pdf

Rapid adaptive radiation of Darwin’s finches depends on ancestral genetic modules

To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of adaptive alleles underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. On a single Bahamian island, ancient standing variation from disjunct geographic sources was reassembled into new combinations under strong directional selection for adaptation to the novel trophic niches of scale-eating and molluscivory. We found evidence for two longstanding hypotheses of adaptive radiation: hybrid swarm origins and temporal stages of adaptation. Using a combination of population genomics, transcriptomics, and genome-wide association mapping, we demonstrate that this microendemic adaptive radiation of novel trophic specialists on San Salvador Island, Bahamas experienced twice as much adaptive introgression as generalist populations on neighboring islands and that adaptive divergence occurred in stages. First, standing regulatory variation in genes associated with feeding behavior (prlh, cfap20, and rmi1) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (itga5, ext1, cyp26b1, and galr2) and finally the only de novo nonsynonymous substitution in an osteogenic transcription factor and oncogene (twist1) swept to fixation most recently. Our results demonstrate how ancient alleles maintained in distinct environmental refugia can be assembled into new adaptive combinations and provide a framework for reconstructing the spatiotemporal landscape of adaptation and speciation.

/pdf/a-vertebrate-adaptive-radiation-is-assembled-from-an-ancient-22rlorcwyv.pdf

A vertebrate adaptive radiation is assembled from an ancient and disjunct spatiotemporal landscape.

Abstract Laboratory studies have demonstrated that a single phenotype can be produced by many different genotypes; however, in natural systems, it is frequently found that phenotypic convergence is due to parallel genetic changes. This suggests a substantial role for constraint and determinism in evolution and indicates that certain mutations are more likely to contribute to phenotypic evolution. Here we use whole genome resequencing in the Mexican tetra, Astyanax mexicanus , to investigate how selection has shaped the repeated evolution of both trait loss and enhancement across independent cavefish lineages. We show that selection on standing genetic variation and de novo mutations both contribute substantially to repeated adaptation. Our findings provide empirical support for the hypothesis that genes with larger mutational targets are more likely to be the substrate of repeated evolution and indicate that features of the cave environment may impact the rate at which mutations occur. 

/pdf/selection-driven-trait-loss-in-independently-evolved-1jhisets.pdf

Selection-driven trait loss in independently evolved cavefish populations

Repeated evolution provides valuable insight into adaptation. In this study, the authors found that repeated evolution of cave-adapted phenotypes of a fish (Astyanax mexicanus) was driven by selection on standing genetic variation and novel mutations and genes repeatedly under selection are longer compared to the rest of the genome. Laboratory studies have demonstrated that a single phenotype can be produced by many different genotypes; however, in natural systems, it is frequently found that phenotypic convergence is due to parallel genetic changes. This suggests a substantial role for constraint and determinism in evolution and indicates that certain mutations are more likely to contribute to phenotypic evolution. Here we use whole genome resequencing in the Mexican tetra, Astyanax mexicanus , to investigate how selection has shaped the repeated evolution of both trait loss and enhancement across independent cavefish lineages. We show that selection on standing genetic variation and de novo mutations both contribute substantially to repeated adaptation. Our findings provide empirical support for the hypothesis that genes with larger mutational targets are more likely to be the substrate of repeated evolution and indicate that features of the cave environment may impact the rate at which mutations occur.

The effect of the environment on fitness in natural populations is a fundamental question in evolutionary biology. However, experimental manipulations of both environment and phenotype at the same time are rare. Thus, the relative importance of the competitive environment versus intrinsic organismal performance in shaping the location, height, and fluidity of fitness peaks and valleys remains largely unknown. Here, we experimentally tested the effect of competitor frequency on the complex fitness landscape driving adaptive radiation of a generalist and two trophic specialist pupfishes, a scale-eater and molluscivore, endemic to hypersaline lakes on San Salvador Island (SSI), Bahamas. We manipulated phenotypes, by generating 3407 F4/F5 lab-reared hybrids, and competitive environment, by altering the frequency of rare transgressive hybrids between field enclosures in two independent lake populations. We then tracked hybrid survival and growth rates across these four field enclosures for 3-11 months. In contrast to competitive speciation theory, we found no evidence that the frequency of hybrid phenotypes affected their survival. Instead, we observed a strikingly similar fitness landscape to a previous independent field experiment, each supporting multiple fitness peaks for generalist and molluscivore phenotypes and a large fitness valley isolating the divergent scale-eater phenotype. These features of the fitness landscape were stable across manipulated competitive environments, multivariate trait axes, and spatiotemporal heterogeneity. We suggest that absolute performance constraints and divergent gene regulatory networks shape macroevolutionary (interspecific) fitness landscapes in addition to microevolutionary (intraspecific) competitive dynamics. This interplay between organism and environment underlies static and dynamic features of the adaptive landscape.

/pdf/surprising-spatiotemporal-stability-of-a-multi-peak-fitness-m47ze0460r.pdf

Surprising spatiotemporal stability of a multi‐peak fitness landscape revealed by independent field experiments measuring hybrid fitness

A computational framework for studying energetics and resource management in sea turtle migration and autonomous systems

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A vertebrate adaptive radiation is assembled from an ancient and disjunct spatiotemporal landscape.

A computational framework for studying energetics and resource management in sea turtle migration and autonomous systems