| 1. |
- Berdan, Emma L, 1983, et al.
(author)
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How chromosomal inversions reorient the evolutionary process
- 2023
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In: Journal of Evolutionary Biology. - 1010-061X .- 1420-9101. ; 36:12, s. 1761-1782
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Research review (peer-reviewed)abstract
- Inversions are structural mutations that reverse the sequence of a chromosome seg-ment and reduce the effective rate of recombination in the heterozygous state. They play a major role in adaptation, as well as in other evolutionary processes such as spe-ciation. Although inversions have been studied since the 1920s, they remain difficult to investigate because the reduced recombination conferred by them strengthens the effects of drift and hitchhiking, which in turn can obscure signatures of selection. Nonetheless, numerous inversions have been found to be under selection. Given re-cent advances in population genetic theory and empirical study, here we review how different mechanisms of selection affect the evolution of inversions. A key difference between inversions and other mutations, such as single nucleotide variants, is that the fitness of an inversion may be affected by a larger number of frequently interacting processes. This considerably complicates the analysis of the causes underlying the evolution of inversions. We discuss the extent to which these mechanisms can be disentangled, and by which approach.
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| 2. |
- Merot, C., et al.
(author)
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Intercontinental karyotype - environment parallelism supports a role for a chromosomal inversion in local adaptation in a seaweed fly
- 2018
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In: Proceedings of the Royal Society B-Biological Sciences. - : The Royal Society. - 0962-8452 .- 1471-2954. ; 285:1881
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Journal article (peer-reviewed)abstract
- 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 specialization. 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 2000 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 to be 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.
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| 3. |
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| 4. |
- Berdan, Emma L, 1983, et al.
(author)
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A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)
- 2021
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In: EVOLUTION LETTERS. - : Oxford University Press (OUP). - 2056-3744. ; 5:6, s. 607-624
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Journal article (peer-reviewed)abstract
- 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, most likely via linked variation, 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 of 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.
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| 5. |
- Berdan, Emma L, 1983, et al.
(author)
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A metabarcoding analysis of the wrackbed microbiome indicates a phylogeographic break along the North Sea-Baltic Sea transition zone
- 2023
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In: Environmental Microbiology. - 1462-2912. ; 25:9, s. 1659-73
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Journal article (peer-reviewed)abstract
- Sandy beaches are biogeochemical hotspots that bridge marine and terrestrial ecosystems via the transfer of 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 this community. 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 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 driven by changes in the frequency of different groups of known polysaccharide degraders. We hypothesize that microbes were selected for their abilities to degrade different polysaccharides corresponding to a shift in polysaccharide content in the different seaweed communities. Our results reveal the complexities of both the wrackbed microbial community, with different groups specialized to different roles, and the cascading trophic consequences of shifts in the near shore algal community.
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| 6. |
- Berdan, Emma L, 1983, et al.
(author)
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Deleterious mutation accumulation and the long-term fate of chromosomal inversions
- 2021
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In: PLoS Genetics. - : Public Library of Science (PLoS). - 1553-7404. ; 17:3
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Journal article (peer-reviewed)abstract
- Author summary A 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. 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.
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| 7. |
- Berdan, Emma L, 1983, et al.
(author)
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Genetic divergence and phenotypic plasticity contribute to variation in cuticular hydrocarbons in the seaweed fly Coelopa frigida
- 2019
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In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 9:21, s. 12156-12170
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Journal article (peer-reviewed)abstract
- Cuticular hydrocarbons (CHCs) form the boundary between insects and their environments and often act as essential cues for species, mate, and kin recognition. This complex polygenic trait can be highly variable both among and within species, but the causes of this variation, especially the genetic basis, are largely unknown. In this study, we investigated phenotypic and genetic variation of CHCs in the seaweed fly, Coelopa frigida, and found that composition was affected by both genetic (sex and population) and environmental (larval diet) factors. We subsequently conducted behavioral trials that show CHCs are likely used as a sexual signal. We identified general shifts in CHC chemistry as well as individual compounds and found that the methylated compounds, mean chain length, proportion of alkenes, and normalized total CHCs differed between sexes and populations. We combined these data with whole genome resequencing data to examine the genetic underpinnings of these differences. We identified 11 genes related to CHC synthesis and found population-level outlier SNPs in 5 that are concordant with phenotypic differences. Together these results reveal that the CHC composition of C. frigida is dynamic, strongly affected by the larval environment, and likely under natural and sexual selection.
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| 8. |
- Berdan, Emma L, 1983, et al.
(author)
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Genomic architecture of supergenes: Connecting form and function
- 2022
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In: Philosophical Transactions of the Royal Society B: Biological Sciences. - : The Royal Society. - 0962-8436 .- 1471-2970. ; 377:1856
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Journal article (peer-reviewed)abstract
- Supergenes are tightly linked sets of loci that are inherited together and control complex phenotypes. While classical supergenes-governing traits such as wing patterns in Heliconius butterflies or heterostyly in Primula-have been studied since the Modern Synthesis, we still understand very little about howthey evolve and persist in nature. The genetic architecture of supergenes is a critical factor affecting their evolutionary fate, as it can change key parameters such as recombination rate and effective population size, potentially redirecting molecular evolution of the supergene in addition to the surrounding genomic region. To understand supergene evolution, we must link genomic architecture with evolutionary patterns and processes. This is now becoming possible with recent advances in sequencing technology and powerful forward computer simulations. The present theme issue brings together theoretical and empirical papers, as well as opinion and synthesis papers, which showcase the architectural diversity of supergenes and connect this to critical processes in supergene evolution, such as polymorphism maintenance and mutation accumulation. Here,we summarize those insights to highlight new ideas and methods that illuminate the path forward for the study of supergenes in nature. This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.
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| 9. |
- Berdan, Emma L, 1983, et al.
(author)
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Genomic landscape of reproductive isolation in Lucania killifish: The role of sex loci and salinity
- 2021
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In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 34:1, s. 157-174
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Journal article (peer-reviewed)abstract
- Adaptation to different environments can directly and indirectly generate reproductive isolation between species. Bluefin killifish (Lucania goodei) and rainwater killifish (L. parva) are sister species that have diverged across a salinity gradient and are reproductively isolated by habitat, behavioural, extrinsic and intrinsic post-zygotic isolation. We asked if salinity adaptation contributes indirectly to other forms of reproductive isolation via linked selection and hypothesized that low recombination regions, such as sex chromosomes or chromosomal rearrangements, might facilitate this process. We conducted QTL mapping in backcrosses between L. parva and L. goodei to explore the genetic architecture of salinity tolerance, behavioural isolation and intrinsic isolation. We mapped traits relative to a chromosome that has undergone a centric fusion in L. parva (relative to L. goodei). We found that the sex locus appears to be male determining (XX-XY), was located on the fused chromosome and was implicated in intrinsic isolation. QTL associated with salinity tolerance were spread across the genome and did not overly co-localize with regions associated with behavioural or intrinsic isolation. This preliminary analysis of the genetic architecture of reproductive isolation between Lucania species does not support the hypothesis that divergent natural selection for salinity tolerance led to behavioural and intrinsic isolation as a by-product. Combined with previous studies in this system, our work suggests that adaptation as a function of salinity contributes to habitat isolation and that reinforcement may have contributed to the evolution of behavioural isolation instead, possibly facilitated by linkage between behavioural isolation and intrinsic isolation loci on the fused chromosome.
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| 10. |
- Berdan, Emma L, 1983, et al.
(author)
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Inversion frequencies and phenotypic effects are modulated by the environment: insights from a reciprocal transplant study in Coelopa frigida
- 2018
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In: Evolutionary Ecology. - : Springer Science and Business Media LLC. - 0269-7653 .- 1573-8477. ; 32:6, s. 683-698
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Journal article (peer-reviewed)abstract
- 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 / 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 (genotypexenvironment effects). Here we use a reciprocal transplant experiment to test the effect of the / 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 populationxsubstrate 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.
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| 11. |
- Berdan, Emma L, 1983, et al.
(author)
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Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals
- 2022
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In: Philosophical Transactions of the Royal Society B-Biological Sciences. - : The Royal Society. - 0962-8436 .- 1471-2970. ; 377:1856
-
Journal article (peer-reviewed)abstract
- Supergenes offer spectacular examples of long-term balancing selection in nature, but their origin and maintenance remain a mystery. Reduced recombination between arrangements, a critical aspect of many supergenes, protects adaptive multi-trait phenotypes but can lead to 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 outcome is the formation of maladaptive balanced lethal systems, where only heterozygotes remain viable and reproduce. We investigated the conditions under which these different outcomes occur, assuming a scenario of introgression after divergence. We found that AOD aided the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism was easily destabilized by further mutation accumulation, which was often asymmetric, disrupting the quasi-equilibrium state. Mechanisms that accelerated degeneration tended to amplify asymmetric mutation accumulation between the supergene arrangements and vice-versa. As the evolution of balanced lethal systems requires symmetric degeneration of both arrangements, this leaves only restricted conditions for their evolution, namely small population sizes and low rates of gene conversion. The dichotomy between the persistence of polymorphism and degeneration of supergene arrangements likely underlies the rarity of balanced lethal systems in nature.This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.
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| 12. |
- Blankers, T., et al.
(author)
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Demography and selection shape transcriptomic divergence in field crickets
- 2018
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In: Evolution. - : Wiley. - 0014-3820. ; 72:3, s. 553-567
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Journal article (peer-reviewed)abstract
- 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 genetic differentiation (empirical F-ST distribution). Concordantly, F-ST-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.
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| 13. |
- Enge, Swantje, et al.
(author)
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A supergene in seaweed flies modulates male traits and female perception
- 2023
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In: Proceedings of the Royal Society B: Biological Sciences. - 0962-8452 .- 1471-2954. ; 290:2008
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Journal article (peer-reviewed)abstract
- Supergenes, tightly linked sets of alleles, offer some of the most spectacular examples of polymorphism persisting under long-term balancing selection. However, we still do not understand their evolution and persistence, especially in the face of accumulation of deleterious elements. Here, we show that an overdominant supergene in seaweed flies, Coelopa frigida, modulates male traits, potentially facilitating disassortative mating and promoting intraspecific polymorphism. Across two continents, the Cf-Inv(1) supergene strongly affected the composition of male cuticular hydrocarbons (CHCs) but only weakly affected CHC composition in females. Using gas chromatography-electroantennographic detection, we show that females can sense male CHCs and that there may be differential perception between genotypes. Combining our phenotypic results with RNA-seq data, we show that candidate genes for CHC biosynthesis primarily show differential expression for Cf-Inv(1) in males but not females. Conversely, candidate genes for odorant detection were differentially expressed in both sexes but showed high levels of divergence between supergene haplotypes. We suggest that the reduced recombination between supergene haplotypes may have led to rapid divergence in mate preferences as well as increasing linkage between male traits, and overdominant loci. Together this probably helped to maintain the polymorphism despite deleterious effects in homozygotes.
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| 14. |
- Gutiérrez-Valencia, Juanita, et al.
(author)
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Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level
- 2022
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In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 32:20, s. 4360-4371, 4371.e1-4371.e6
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Journal article (peer-reviewed)abstract
- Supergenes govern multi-trait-balanced polymorphisms in a wide range of systems; however, our understanding of their origins and evolution remains incomplete. The reciprocal placement of stigmas and anthers in pin and thrum floral morphs of distylous species constitutes an iconic example of a balanced polymorphism governed by a supergene, the distyly S-locus. Recent studies have shown that the Primula and Turnera distyly supergenes are both hemizygous in thrums, but it remains unknown whether hemizygosity is pervasive among distyly S-loci. As hemizygosity has major consequences for supergene evolution and loss, clarifying whether this genetic architecture is shared among distylous species is critical. Here, we have characterized the genetic architecture and evolution of the distyly supergene in Linum by generating a chromosome-level genome assembly of Linum tenue, followed by the identification of the S-locus using population genomic data. We show that hemizygosity and thrum-specific expression of S-linked genes, including a pistil-expressed candidate gene for style length, are major features of the Linum S-locus. Structural variation is likely instrumental for recombination suppression, and although the non-recombining dominant haplotype has accumulated transposable elements, S-linked genes are not under relaxed purifying selection. Our findings reveal remarkable convergence in the genetic architecture and evolution of independently derived distyly supergenes, provide a counterexample to classic inversion-based supergenes, and shed new light on the origin and maintenance of an iconic floral polymorphism.
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| 15. |
- Hyndes, G. A., et al.
(author)
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The role of inputs of marine wrack and carrion in sandy-beach ecosystems: a global review
- 2022
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In: Biological Reviews Cambridge Philosophical Society. - : Wiley. - 1464-7931 .- 1469-185X. ; 97:6, s. 2127-61
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Research review (peer-reviewed)abstract
- Sandy beaches are iconic interfaces that functionally link the ocean with the land via the flow of organic matter from the sea. These cross-ecosystem fluxes often comprise uprooted seagrass and dislodged macroalgae that can form substantial accumulations of detritus, termed 'wrack', on sandy beaches. In addition, the tissue of the carcasses of marine animals that regularly wash up on beaches form a rich food source ('carrion') for a diversity of scavenging animals. Here, we provide a global review of how wrack and carrion provide spatial subsidies that shape the structure and functioning of sandy-beach ecosystems (sandy beaches and adjacent surf zones), which typically have little in situ primary production. We also examine the spatial scaling of the influence of these processes across the broader land- and seascape, and identify key gaps in our knowledge to guide future research directions and priorities. Large quantities of detrital kelp and seagrass can flow into sandy-beach ecosystems, where microbial decomposers and animals process it. The rates of wrack supply and its retention are influenced by the oceanographic processes that transport it, the geomorphology and landscape context of the recipient beaches, and the condition, life history and morphological characteristics of the macrophyte taxa that are the ultimate source of wrack. When retained in beach ecosystems, wrack often creates hotspots of microbial metabolism, secondary productivity, biodiversity, and nutrient remineralization. Nutrients are produced during wrack breakdown, and these can return to coastal waters in surface flows (swash) and aquifers discharging into the subtidal surf. Beach-cast kelp often plays a key trophic role, being an abundant and preferred food source for mobile, semi-aquatic invertebrates that channel imported algal matter to predatory invertebrates, fish, and birds. The role of beach-cast marine carrion is likely to be underestimated, as it can be consumed rapidly by highly mobile scavengers (e.g. foxes, coyotes, raptors, vultures). These consumers become important vectors in transferring marine productivity inland, thereby linking marine and terrestrial ecosystems. Whilst deposits of organic matter on sandy-beach ecosystems underpin a range of ecosystem functions and services, they can be at variance with aesthetic perceptions resulting in widespread activities, such as 'beach cleaning and grooming'. This practice diminishes the energetic base of food webs, intertidal fauna, and biodiversity. Global declines in seagrass beds and kelp forests (linked to global warming) are predicted to cause substantial reductions in the amounts of marine organic matter reaching many beach ecosystems, likely causing flow-on effects for food webs and biodiversity. Similarly, future sea-level rise and increased storm frequency are likely to alter profoundly the physical attributes of beaches, which in turn can change the rates at which beaches retain and process the influxes of wrack and animal carcasses. Conservation of the multi-faceted ecosystem services that sandy beaches provide will increasingly need to encompass a greater societal appreciation and the safeguarding of ecological functions reliant on beach-cast organic matter on innumerable ocean shores worldwide.
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| 16. |
- Rigby, Kristie, 1987, et al.
(author)
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Species Specific Responses to Grazer Cues and Acidification in Phytoplankton- Winners and Losers in a Changing World
- 2022
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In: Frontiers in Marine Sceince. - : Frontiers Media SA. - 2296-7745. ; 9
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Journal article (peer-reviewed)abstract
- Phytoplankton induce defensive traits in response to chemical alarm signals from grazing zooplankton. However, these signals are potentially vulnerable to changes in pH and it is not yet known how predator recognition may be affected by ocean acidification. We exposed four species of diatoms and one toxic dinoflagellate to futurepCO2levels, projected by the turn of the century, in factorial combinations with predatory cues from copepods (copepodamides). We measured the change in growth, chain length, silica content, and toxin content. Effects of increasedpCO2were highly species specific. The induction of defensive traits was accompanied by a significant reduction in growth rate in three out of five species. The reduction averaged 39% and we interpret this as an allocation cost associated with defensive traits. Copepodamides induced significant chain length reduction in three of the four diatom species. Under elevatedpCO2Skeletonema marinoireduced silica content by 30% and inAlexandrium minutumthe toxin content was reduced by 30%. Using copepodamides to induce defensive traits in the absence of direct grazing provides a straightforward methodology to assess costs of defense in microplankton. We conclude that copepodamide signalling system is likely robust to ocean acidification. Moreover, the variable responses of different taxa to ocean acidification suggest that there will be winners and losers in a highpCO2world, and that ocean acidification may have structuring effects on phytoplankton communities.
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