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Berdan, E.

Publications and source records attributed to Berdan, E..

9 recordsLinked to original sources

Supergene degeneration opposes polymorphism: The curious case of balanced lethals

Supergenes offer some of the most spectacular examples of long-term balancing selection in nature but their origin and maintenance remain a mystery. A critical aspect of supergenes is reduced recombination between arrangements. Reduced recombination protects adaptive multi-trait phenotypes, but can also lead to degeneration through mutation accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes. One such outcome is the formation of balanced lethal systems, a maladaptive system where both supergene arrangements have accumulated deleterious mutations to the extent that both homozygotes are inviable, leaving only heterozygotes to reproduce. Here, we perform a simulation study to understand the conditions under which these different outcomes occur, assuming a scenario of introgression after allopatric divergence. We found that AOD aids the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism is easily destabilized by further mutation accumulation. While degradation may strengthen AOD, thereby stabilizing the supergene polymorphism, it is often asymmetric, which is the key disrupter of the quasi-equilibrium state of the polymorphism. Furthermore, mechanisms that accelerate degeneration also tend to amplify asymmetric mutation accumulation between the supergene arrangements and vice versa. As the evolution of a balanced lethal system requires symmetric degradation of both arrangements, this leaves highly restricted conditions under which such a system could evolve. We show that small population size and low dominance coefficients are critical factors, as these reduce the efficacy of selection. The dichotomy between the persistence of a polymorphism and degradation of supergene arrangements likely underlies the rarity of balanced lethal systems in nature.

evolutionary biology↗

A metagenomic analysis of the wrackbed microbiome indicates a phylogeographic break along the North Sea - Baltic Sea transition zone

Sandy beaches are biogeochemical hotspots that bridge marine and terrestrial ecosystems via the transfer of marine organic matter, such as seaweed (termed wrack). A keystone of this unique ecosystem is the microbial community, which helps to degrade wrack and re-mineralize nutrients. However, little is known about the wrackbed microbiome, its composition, trophic ecology, or how it varies over time and space. Here we characterize the wrackbed microbiome as well as the microbiome of a primary consumer, the seaweed fly Coelopa frigida, and examine how they change along one of the most studied ecological gradients in the world, the transition from the marine North Sea to the brackish Baltic Sea. We found that polysaccharide degraders dominated both the wrackbed and seaweed fly microbiomes but there were still consistent differences between wrackbed and fly samples. Furthermore, we observed a shift in both microbial communities and functionality between the North and Baltic Sea. These shifts were mostly due to changes in the frequency of different groups of known polysaccharide degraders (Proteobacteria and Bacteroidota). We hypothesize that microbes were selected for their abilities to degrade different polysaccharides corresponding to a shift in polysaccharide content in the seaweed communities of the North vs. Baltic Sea. Our results reveal the complexities of both the wracked microbial community, with different groups specialized to different roles, and the cascading trophic consequences of shifts in the near shore algal community.

genomics↗

A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)

Inversions often underlie complex adaptive traits, but the genic targets inside them are largely unknown. Gene expression profiling provides a powerful way to link inversions with their phenotypic consequences. We examined the effects of the Cf-Inv(1) inversion in the seaweed fly Coelopa frigida on gene expression variation across sexes and life stages. Our analyses revealed that Cf-Inv(1) shapes global expression patterns but the extent of this effect is variable with much stronger effects in adults than larvae. Furthermore, within adults, both common as well as sex specific patterns were found. The vast majority of these differentially expressed genes mapped to Cf-Inv(1). However, genes that were differentially expressed in a single context (i.e. in males, females or larvae) were more likely to be located outside of Cf-Inv(1). By combining our findings with genomic scans for environmentally associated SNPs, we were able to pinpoint candidate variants in the inversion that may underlie mechanistic pathways that determine phenotypes. Together the results in this study, combined with previous findings, support the notion that the polymorphic Cf-Inv(1) inversion in this species is a major factor shaping both coding and regulatory variation resulting in highly complex adaptive effects.

evolutionary biology↗

Chromosomal rearrangements represent modular cassettes for local adaptation across different geographic scales

Across a species range, multiple sources of environmental heterogeneity, at both small and large scales, create complex landscapes of selection, which may challenge adaptation, particularly when gene flow is high. One key to multidimensional adaptation may reside in the heterogeneity of recombination along the genome. Structural variants, like chromosomal inversions, reduce recombination, increasing linkage disequilibrium among loci at a potentially massive scale. In this study, we examined how chromosomal inversions shape genetic variation across a species range, and ask how their contribution to adaptation in the face of gene flow varies across geographic scales. We sampled the seaweed fly Coelopa frigida along a bioclimatic gradient stretching across 10{degrees} of latitude, a salinity gradient and a range of heterogeneous, patchy habitats. We generated a chromosome-level genome assembly to analyse 1,446 low-coverage whole genomes collected along those gradients. We found several large non-recombining genomic regions, including putative inversions. In contrast to the collinear regions, inversions and low recombining regions differentiated populations more strongly, either along an ecogeographic cline or at a fine-grained scale. These genomic regions were associated with environmental factors and adaptive phenotypes, albeit with contrasting patterns. Altogether, our results highlight the importance of recombination in shaping adaptation to environmental heterogeneity at local and large scales.

evolutionary biology↗

Genomic landscape of reproductive isolation in Lucania killifish: The role of sex chromosomes and salinity

Understanding how speciation occurs and how reproductive barriers contribute to population structure at a genomic scale requires elucidating the genetic architecture of reproductive isolating barriers. In particular, it is crucial to determine if loci underlying reproductive isolation are genetically linked or if they are located on sex chromosomes, which have unique inheritance and population genetic properties. Bluefin killifish (Lucania goodei) and rainwater killifish (L. parva) are closely related species that have diverged across a salinity gradient and are reproductively isolated by assortative mating, hybrid male infertility, viability of hybrid offspring at high salinities, as well as reduced overall fitness of F2 offspring and backcrosses to L. goodei. We conducted QTL mapping in backcrosses between L. parva and L. goodei to determine the genetic architecture of sex determination, mate attractiveness, fertility, and salinity tolerance. We find that the sex locus appears to be male determining and located on a chromosome that has undergone a Robertsonian fusion in L. parva relative to L. goodei. We find that the sex locus on the fused chromosome is involved in several genomic incompatibilities, which affect the survival of backcrossed offspring. Among the backcrossed offspring that survived to adulthood, we find that one QTL for male attractiveness to L. goodei females is closely linked to this sex locus on chromosome 1. Males homozygous for L. goodei alleles at the sex locus laid more eggs with L. goodei females. QTL associated with salinity tolerance were spread across the genome but did not tend to co-localize with reproductive isolation. Thus, speciation in this system appears to be driven by reinforcement and indirect selection against hybrids rather than direct natural selection for salinity tolerance. Our work adds to growing evidence that sex chromosome evolution may contribute to speciation.

evolutionary biology↗

Muller’s Ratchet and the Long-Term Fate of Chromosomal Inversions

Chromosomal inversions contribute widely to adaptation and speciation, yet they present a unique evolutionary puzzle as both their allelic content and frequency evolve in a feedback loop. In this simulation study, we quantified the role of the allelic content in determining the long-term fate of the inversion. Recessive deleterious mutations accumulated on both arrangements with most of them being private to a given arrangement. This led to increasing overdominance, allowing for the maintenance of the inversion polymorphism and generating strong non-adaptive divergence between arrangements. The accumulation of mutations was mitigated by gene conversion but nevertheless led to the fitness decline of at least one homokaryotype under all considered conditions. Surprisingly, this fitness degradation could be permanently halted by the branching of an arrangement into multiple highly divergent haplotypes. Our results highlight the dynamic features of inversions by showing how the non-adaptive evolution of allelic content can play a major role in the fate of the inversion. Author SummaryA chromosomal inversion is a segment of the chromosome that is flipped (inverted arrangement) relative to the normal orientation (standard arrangement). Such structural mutations may facilitate evolutionary processes such as adaptation and speciation, because reduced recombination in inverted regions allows beneficial combinations of alleles to behave as a "single unit". This locally reduced recombination can have major consequences for the evolution of the allelic content inside the inversion. We used simulations to investigate some of these consequences. Inverted regions tended to accumulate more deleterious recessive mutations than the rest of the genome, which decreased the fitness of homokarotypes (individuals with two copies of the same arrangement). This led to a strong selective advantage for heterokaryotypes (individuals with one copy of each arrangement), maintaining the inversion polymorphism in the population. The accumulation of deleterious mutations also resulted in strong divergence between arrangements. We occasionally observed an arrangement that diverged into a small number of highly differentiated haplotypes, stopping the fitness decrease in homokaryotypes. Our results highlight the dynamic features of inversions by showing how the evolution of allelic content can greatly affect the fate of an inversion.

evolutionary biology↗

Inversion frequencies and phenotypic effects are modulated by the environment

Understanding how environmental variation drives phenotypic diversification within species is a major objective in evolutionary biology. The seaweed fly Coelopa frigida provides an excellent model for the study of genetically driven phenotypes because it carries an /{beta} inversion polymorphism that affects body size. Coelopa frigida inhabits highly variable beds of decomposing seaweed on the coast in Scandinavia thus providing a suitable test ground to investigate the genetic effects of substrate on both the frequency of the inversion (directional selection) and on the phenotype (genotype x environment effects). Here we use a reciprocal transplant experiment to test the effect of the /{beta} inversion on body size traits and development time across four suitable natural breeding substrates from the clinal distribution. We show that while development time is unaffected by GxE effects, both the frequency of the inversion and the relative phenotypic effects of the inversion on body size differ between population x substrate combinations. This indicates that the environment modulates the fitness as well as the phenotypic effects of the inversion karyotypes. It further suggests that the inversion may have accumulated qualitatively different mutations in different populations that interact with the environment. Together our results are consistent with the idea that the inversion in C. frigida likely evolves via a combination of local mutation, GxE effects, and differential fitness of inversion karyotypes in heterogeneous environments.

evolutionary biology↗

Karyotype-environment associations support a role for a chromosomal inversion in local adaptation among North American populations of the seaweed fly Coelopa frigida

Large chromosomal rearrangements are thought to facilitate adaptation to heterogeneous environments by limiting genomic recombination. Indeed, inversions have been implicated in adaptation along environmental clines and in ecotype specialisation. Here, we combine classical ecological studies and population genetics to investigate an inversion polymorphism previously documented in Europe among natural populations of the seaweed fly Coelopa frigida along a latitudinal cline in North America. We test if the inversion is present in North America and polymorphic, assess which environmental conditions modulate the inversion karyotype frequencies, and document the relationship between inversion karyotype and adult size. We sampled nearly 2,000 flies from 20 populations along several environmental gradients to quantify associations of inversion frequencies to heterogeneous environmental variables. Genotyping and phenotyping showed a widespread and conserved inversion polymorphism between Europe and America. Variation in inversion frequency was significantly associated with environmental factors, with parallel patterns between continents, indicating that the inversion may play a role in local adaptation. The three karyotypes of the inversion are differently favoured across micro-habitats and represent life-history strategies likely maintained by the collective action of several mechanisms of balancing selection. Our study adds to the mounting evidence that inversions are facilitators of adaptation and enhance within-species diversity.

evolutionary biology↗

Demography and selection shape transcriptomic divergence in field crickets

Gene flow, demography, and selection can result in similar patterns of genomic variation and disentangling their effects is key to understanding speciation. Here, we assess transcriptomic variation to unravel the evolutionary history of Gryllus rubens and Gryllus texensis, cryptic field cricket species with highly divergent mating behavior. We infer their demographic history and screen their transcriptomes for footprints of selection in the context of the inferred demography. We find strong support for a long history of bidirectional gene flow, which ceased during the late Pleistocene, and a bottleneck in G. rubens consistent with a peripatric origin of this species. Importantly, the demographic history has likely strongly shaped patterns of neutral genetic differentiation (empirical FST distribution). Concordantly, FST based selection detection uncovers a large number of outliers, likely comprising many false positives, echoing recent theoretical insights. Alternative genetic signatures of positive selection, informed by the demographic history of the sibling species, highlighted a smaller set of loci; many of these are candidates for controlling variation in mating behavior. Our results underscore the importance of demography in shaping overall patterns of genetic divergence and highlight that examining both demography and selection facilitates a more complete understanding of genetic divergence during speciation.

evolutionary biology↗