Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for 'pin' and 'thrum' floral types in Primula and Fagopyrum, but classic examples are also found in insect mimicry and snail morphology. Understanding the evolutionary mechanisms that generate these co-adapted gene sets, as well as the mode of limiting the production of unfit recombinant forms, remains a substantial challenge. Here we show that individual wing-pattern morphs in the polymorphic mimetic butterfly Heliconius numata are associated with different genomic rearrangements at the supergene locus P. These rearrangements tighten the genetic linkage between at least two colour-pattern loci that are known to recombine in closely related species, with complete suppression of recombination being observed in experimental crosses across a 400-kilobase interval containing at least 18 genes. In natural populations, notable patterns of linkage disequilibrium (LD) are observed across the entire P region. The resulting divergent haplotype clades and inversion breakpoints are found in complete association with wing-pattern morphs. Our results indicate that allelic combinations at known wing-patterning loci have become locked together in a polymorphic rearrangement at the P locus, forming a supergene that acts as a simple switch between complex adaptive phenotypes found in sympatry. These findings highlight how genomic rearrangements can have a central role in the coexistence of adaptive phenotypes involving several genes acting in concert, by locally limiting recombination and gene flow.

Frequent extinctions of local populations in metapopulations create opportunities for migrant females to establish new populations. In a metapopulation of the Glanville fritillary butterfly (Melitaea cinxia), more mobile individuals are more likely to establish new populations, especially in habitat patches that are poorly connected to existing populations. Here we show that flight metabolic rate and the frequency of a specific allele of the metabolic enzyme phosphoglucose isomerase ( pgi ) were both highest in newly established, isolated populations. Furthermore, genotypes with this pgi allele had elevated flight metabolic rates. These results suggest that genetic variation in pgi or a closely linked locus has a direct effect on flight metabolism, dispersal rate, and thereby on metapopulation dynamics in this species. These results also contribute to an emerging understanding of the mechanisms by which population turnover in heterogeneous landscapes may maintain genetic and phenotypic variation across populations.

Immigrants to habitats occupied by conspecific organisms are usually expected to be competitively inferior, because residents may be locally adapted. If residents are inbred, however, mating between immigrants and residents results in offspring that may enjoy a fitness advantage from hybrid vigor. We demonstrate this effect experimentally in a natural Daphnia metapopulation in which genetic bottlenecks and local inbreeding are common. We estimate that in this metapopulation, hybrid vigor amplifies the rate of gene flow several times more than would be predicted from the nominal migration rate. This can affect the persistence of local populations and the entire metapopulation.

If colonization of empty habitat patches causes genetic bottlenecks, freshly founded, young populations should be genetically less diverse than older ones that may have experienced successive rounds of immigration. This can be studied in metapopulations with subpopulations of known age. We studied allozyme variation in metapopulations of two species of water fleas (Daphnia) in the skerry archipelago of southern Finland. These populations have been monitored since 1982. Screening 49 populations of D. longispina and 77 populations of D. magna, separated by distances of 1.5-2180 m, we found that local genetic diversity increased with population age whereas pairwise differentiation among pools decreased with population age. These patterns persisted even after controlling for several potentially confounding ecological variables, indicating that extinction and recolonization dynamics decrease local genetic diversity and increase genetic differentiation in these metapopulations by causing genetic bottlenecks during colonization. We suggest that the effect of these bottlenecks may be twofold, namely decreasing genetic diversity by random sampling and leading to population-wide inbreeding. Subsequent immigration then may not only introduce new genetic material, but also lead to the production of noninbred hybrids, selection for which may cause immigrant alleles to increase in frequency, thus leading to increased genetic diversity in older populations. M ANY populations exist as metapopulations, that dynamics affect genetic diversity has received less attenis, as populations structured into interconnected tion. Theory predicts that turnover dynamics mostly demes with local "turnover" dynamics of extinction and (but not invariably) lead to increased genetic differentirecolonization (Andrewartha and Birch 1954; Hanation and decreased local genetic diversity as compared ski 1999). Evolutionary processes in metapopulations to similarly structured populations without extinction differ in many aspects from those in large, uniform popand recolonization dynamics (Slatkin 1977; Wade and ulations because gene flow among demes is restricted, McCauley 1988; Whitlock and McCauley 1990; local demes may be small, and turnover dynamics lead Austerlitz et al. 1997Austerlitz et al. , 2000; Le Corre and Kremer to genetic bottlenecks during recolonization (Andrew-1998;Pannell and Charlesworth 1999). artha and Birch 1954; Hanski and Gilpin 1997; HanThis can be studied empirically in metapopulations ski 1999). Moreover, metapopulation structure may be in which the age of local demes is known. If turnover important for evolutionary processes even in populadynamics increase genetic differentiation, young demes tions that do not exist as ecological metapopulations should be more strongly differentiated than old demes, (i.e., with turnover dynamics too weak to influence debecause age structure in metapopulations is a direct mography). This is because many migrants are needed consequence of turnover. Indeed, a number of empirito homogenize...

One contribution of 15 to a theme issue 'Weird sex: the underappreciated diversity of sexual reproduction'. Meiosis is a key event of sexual life cycles in eukaryotes. Its mechanistic details have been uncovered in several model organisms, and most of its essential features have received various and often contradictory evolutionary interpretations. In this perspective, we present an overview of these often 'weird' features. We discuss the origin of meiosis (origin of ploidy reduction and recombination, two-step meiosis), its secondary modifications (in polyploids or asexuals, inverted meiosis), its importance in punctuating life cycles (meiotic arrests, epigenetic resetting, meiotic asymmetry, meiotic fairness) and features associated with recombination (disjunction constraints, heterochiasmy, crossover interference and hotspots). We present the various evolutionary scenarios and selective pressures that have been proposed to account for these features, and we highlight that their evolutionary significance often remains largely mysterious. Resolving these mysteries will likely provide decisive steps towards understanding why sex and recombination are found in the majority of eukaryotes.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.

Allozyme variation at the phosphoglucose isomerase (PGI) locus in the Glanville fritillary butterfly (Melitaea cinxia) is associated with variation in flight metabolic rate, dispersal rate, fecundity and local population growth rate. To map allozyme to DNA variation and to survey putative functional variation in genomic DNA, we cloned the coding sequence of Pgi and identified nonsynonymous variable sites that determine the most common allozyme alleles. We show that these single‐nucleotide polymorphisms (SNPs) exhibit significant excess of heterozygotes in field‐collected population samples as well as in laboratory crosses. This is in contrast to previous results for the same species in which other allozymes and SNPs were in Hardy–Weinberg equilibrium or exhibited an excess of homozygotes. Our results suggest that viability selection favours Pgi heterozygotes. Although this is consistent with direct overdominance at Pgi, we cannot exclude the possibility that heterozygote advantage is caused by the presence of one or more deleterious alleles at linked loci.

The full exploration of gene-environment interactions requires model organisms with well-characterized ecological interactions in their natural environment, manipulability in the laboratory and genomic tools. The waterflea Daphnia magna is an established ecological and toxicological model species, central to the food webs of freshwater lentic habitats and sentinel for water quality. Its tractability and cyclic parthenogenetic life-cycle are ideal to investigate links between genes and the environment. Capitalizing on this unique model system, the STRESSFLEA consortium generated a comprehensive RNA-Seq data set by exposing two inbred genotypes of D. magna and a recombinant cross of these genotypes to a range of environmental perturbations. Gene models were constructed from the transcriptome data and mapped onto the draft genome of D. magna using EvidentialGene. The transcriptome data generated here, together with the available draft genome sequence of D. magna and a high-density genetic map will be a key asset for future investigations in environmental genomics.

The genetic structure of metapopulations offers insights into the genetic consequences of local extinction and recolonization. We studied allozyme variation in rock pool metapopulations of two species of waterfleas (Daphnia) with the aim to understand how these dynamics influence genetic differentiation. We screened 138 populations of D. magna and 65 populations of D. longispina from an area in the archipelago of southern Finland. The pools from which they were sampled are separated by distances between 1.5 and 4710 m and located on a total of 38 islands. The genetic population structure of the two species was strikingly similar, consistent with their similar metapopulation ecology. The mean F PT value (differentiation among pools with respect to the total metapopulation) was 0.55 and a hierarchical analysis showed that genetic differentiation was strong (40.25) among pools within islands as well as among whole islands. Within islands, pairwise genetic differentiation increased with geographic distance, indicating isolation by distance due to spatially limited dispersal. Previous studies have shown strong founder events occurring during colonization in our metapopulation. We suggest that the genetic population structure in the studied metapopulations is largely explained by three consequences of these founder events: (i) strong drift during colonization, (ii) local inbreeding, which results in hybrid vigour and increased effective migration rates after subsequent immigration, and (iii) effects of selection through hitchhiking of neutral genes with linked loci under selection.