Fine-scale habitat heterogeneity favours the coexistence of supergene-controlled social forms in Formica selysi

Background Social insects vary widely in social organization, yet the genetical and ecological factors influencing this variation remain poorly known. In particular, whether spatially varying selection influences the maintenance of social polymorphisms in ants has been rarely investigated. To fill this gap, we examined whether fine-scale habitat heterogeneity contributes to the co-existence of alternative forms of social organization within populations. Single-queen colonies (monogyne social form) are generally associated with better colonization abilities, whereas multiple-queen colonies (polygyne social form) are predicted to be better competitors and monopolize saturated habitats. We hypothesize that each social form colonizes and thrives in distinct local habitats, as a result of their alternative dispersal and colony founding strategies. Here, we test this hypothesis in the Alpine silver ant, in which a supergene controls polymorphic social organization. Results Monogyne and polygyne colonies predominate in distinct habitats of the same population. The analysis of 59 sampling plots distributed across six habitats revealed that single-queen colonies mostly occupy unconnected habitats that were most likely reached by flight. This includes young habitats isolated by water and old habitats isolated by vegetation. In contrast, multiple-queen colonies were abundant in young, continuous and saturated habitats. Hence, alternative social forms colonize and monopolize distinct niches at a very local scale. Conclusions Alternative social forms colonized and monopolized different local habitats, in accordance with differences in colonization and competition abilities. The monogyne social form displays a colonizer phenotype, by efficiently occupying empty habitats, while the polygyne social form exhibits a competitor phenotype, thriving in saturated habitats. The combination of the two phenotypes, coupled with fine-scale habitat heterogeneity, may allow the coexistence of alternative social forms within populations. Overall, these results suggest that spatially varying selection may be one of the mechanisms contributing to the maintenance of genetic polymorphisms in social organization.

Environmental specialization and cryptic genetic divergence in two massive coral species from the Florida Keys Reef Tract

ABSTRACTBroadcast-spawning coral species have wide geographic ranges, spanning strong environmental gradients, but it is unclear how much spatially varying selection these gradients actually impose. Strong divergent selection might present a considerable barrier for demographic exchange between disparate reef habitats. We investigated whether the cross-shelf gradient (nearshore - offshore - deep) is associated with spatially varying selection in two common coral species, Montastraea cavernosa and Siderastrea siderea, in the Florida Keys. Toward this end, we generated a de novo genome assembly for M. cavernosa and used 2bRAD to genotype 20 juveniles and 20 adults of both species from each of the three reef zones to identify signatures of selection occurring within a single generation. Unexpectedly, each species was found to be composed of four genetically distinct lineages, with gene flow between them still ongoing but highly reduced in 13.0-54.7% of the genome. Each species includes two sympatric lineages that are only found in the deep (20 m) habitat, while the other lineages are found almost exclusively on the shallower reefs (3-10 m). The two “shallow” lineages of M. cavernosa are also specialized for either nearshore or offshore: comparison between adult and juvenile cohorts indicates that cross-shelf migrants are more than twice as likely to die before reaching adulthood than local recruits. Siderastrea siderea and M. cavernosa are among the most ecologically successful species on the degraded Florida Keys Reef Tract, and this work offers important insight on the genomic background of divergent selection and environmental specialization that may in part explain their resilience and broad environmental range.

Global adaptation confounds the search for local adaptation

Spatially varying selection promotes variance in allele frequencies, increasing genetic differentiation between the demes of a metapopulation. For that reason, outliers in the genome wide distribution of summary statistics measuring genetic differentiation, such as FST, are often interpreted as evidence for alleles which contribute to local adaptation. However, in spatially structured populations, the spread of beneficial mutations with spatially uniform effects can also induce transient genetic differentiation and numerous theoretical studies have suggested that species-wide, or global, adaptation makes a substantial contribution to molecular evolution. In this study, we ask whether such global adaptation affects the genome-wide distribution of FST and generates statistical outliers which could be mistaken for local adaptation. Using forward-in-time population genetic simulations assuming parameters for the rate and strength of beneficial mutations similar to those that have been estimated for natural populations, we show the spread of globally beneficial in parapatric populations can readily generate FST outliers, which may be misinterpreted as evidence for local adaptation. The spread of beneficial mutations causes selective sweeps at flanking sites, so the effects of global versus local adaptation may be distinguished by examining patterns of nucleotide diversity along with FST. Our study suggests that global adaptation should be considered in the interpretation of genome-scan results and the design of future studies aimed at understanding the genetic basis of local adaptation.

Local adaptation and the evolution of inversions on sex chromosomes and autosomes

Spatially varying selection with gene flow can favour the evolution of inversions that bind locally adapted alleles together, facilitate local adaptation and ultimately drive genomic divergence between species. Several studies have shown that the rates of spread and establishment of new inversions capturing locally adaptive alleles depend on a suite of evolutionary factors, including the strength of selection for local adaptation, rates of gene flow and recombination, and the deleterious mutation load carried by inversions. Because the balance of these factors is expected to differ between X (or Z) chromosomes and autosomes, opportunities for inversion evolution are likely to systematically differ between these genomic regions, though such scenarios have not been formally modelled. Here, we consider the evolutionary dynamics of X-linked and autosomal inversions in populations evolving at a balance between migration and local selection. We identify three factors that lead to asymmetric rates of X-linked and autosome inversion establishment: (1) sex-biased migration, (2) dominance of locally adapted alleles and (3) chromosome-specific deleterious mutation loads. This theory predicts an elevated rate of fixation, and depressed opportunities for polymorphism, for X-linked inversions. Our survey of data on the genomic distribution of polymorphic and fixed inversions supports both theoretical predictions. This article is part of the theme issue ‘Linking local adaptation with the evolution of sex differences'.

Major QTL controls adaptation to serpentine soils in Mimulus guttatus

ABSTRACTSpatially varying selection is a critical driver of adaptive differentiation. Yet, there are few examples where the fitness effects of naturally segregating variants that contribute to local adaptation have been measured in the field. This project investigates the genetic basis of adaption to serpentine soils in Mimulus guttatus. Reciprocal transplant studies show that serpentine and non-serpentine populations of M. guttatus are genetically differentiated in their ability to survive on serpentine soils. We mapped serpentine tolerance by performing a bulk segregant analysis on F2 survivors from a field transplant study and identify a single QTL where individuals that are homozygous for the non-serpentine allele do not survive on serpentine soils. This same QTL controls serpentine tolerance in a second, geographically distant population. A common garden study where the two serpentine populations were grown on each other′s soil finds that one of the populations has significantly lower survival on this “foreign” serpentine soil compared to its home soil. So, while these two populations share a major QTL they either differ at other loci involved in serpentine adaptation or have different causal alleles at this QTL. This raises the possibility that serpentine populations may not be broadly tolerant to serpentine soils but may instead be locally adapted to their particular patch. Nevertheless, despite the myriad chemical and physical challenges that plants face in serpentine habitats, adaptation to these soils in M. guttatus has a simple genetic basis.

Genome-wide patterns of local adaptation in Drosophila melanogaster: adding intra European variability to the map

ABSTRACTSignatures of spatially varying selection have been investigated both at the genomic and transcriptomic level in several organisms. In Drosophila melanogaster, the majority of these studies have analyzed North American and Australian populations, leading to the identification of several loci and traits under selection. However, populations in these two continents showed evidence of admixture that likely contributed to the observed population differentiation patterns. Thus, disentangling demography from selection is challenging when analyzing these populations. European populations could be a suitable system to identify loci under spatially varying selection provided that no recent admixture from African populations would have occurred. In this work, we individually sequence the genome of 42 European strains collected in populations from contrasting environments: Stockholm (Sweden), and Castellana Grotte, (Southern Italy). We found low levels of population structure and no evidence of recent African admixture in these two populations. We thus look for patterns of spatially varying selection affecting individual genes and gene sets. Besides single nucleotide polymorphisms, we also investigate the role of transposable elements in local adaptation. We concluded that European populations are a good dataset to identify loci under spatially varying selection. The analysis of the two populations sequenced in this work in the context of all the available D. melanogaster data allowed us to pinpoint genes and biological processes relevant for local adaptation. Identifying and analyzing populations with low levels of population structure and admixture should help to disentangle selective from non-selective forces underlying patterns of population differentiation in other species as well.

Sex-dependent dominance at a single locus maintains variation in age at maturity in Atlantic salmon

Males and females share many traits that have a common genetic basis, however selection on these traits often differs between the sexes leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite intense theoretical and empirical interest, the specific genetic loci behind sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution and the maintenance of genetic diversity. Here, we identify a large effect locus controlling age at maturity in 57 salmon populations, an important fitness trait in which selection favours earlier maturation in males than females, and show it is a clear example of sex dependent dominance reducing intralocus sexual conflict and maintaining adaptive variation in wild populations. Using high density SNP data and whole genome re-sequencing, we found that vestigial-like family member 3 (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39.4% of phenotypic variation, an unexpectedly high effect size for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection. Our results provide the first empirical example of dominance reversal permitting greater optimisation of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We further anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed