Biology subjects

Runemark, A.

Publications and source records attributed to Runemark, A..

13 recordsLinked to original sources

bioRxiv2024

Species-specific loss of genetic diversity and accumulation of genetic load following agricultural intensification

Land-use change from agricultural intensification is a major driver of global insect declines. We investigated the genetic consequences of grassland decline in Sweden by sequencing museum and modern specimens of three focal and five additional Polyommatinae butterfly species. From 59 historical and 90 contemporary genomes, we find a 6% decline in genetic diversity and increased isolation and inbreeding in the grassland specialist Cyaniris semiargus over the past 70 years. In contrast, generalist Polyommatus icarus and heathland specialist Plebejus argus maintained genetic diversity and connectivity. Although currently genomic erosion is mild, we infer it lags considerably larger declines in effective population sizes. Using simulations, we demonstrate that only a small portion of genetic diversity is lost in early stages of decline, creating a genetic extinction debt. Two of five additional species show similar reductions, underscoring that restoration of grassland habitat is necessary to restore gene flow and halt further genomic erosion in grassland insects.

genomics↗

bioRxiv2024

Evolved and plastic gene expression in adaptation to a novel niche

Gene expression, resulting from complex regulatory interactions, plays an important role in adaptation and speciation. While gene expression historically has been studied in the context of reproductive isolation in speciation research, a role for evolved differences in gene expression in adaptation to novel niches is increasingly appreciated. How gene expression evolves and enables divergent ecological adaptation, and how changes in gene expression relate to genomic architecture and genetic divergence are pressing questions in understanding the processes of adaptation and ecological speciation. Further, how plasticity in gene expression can both contribute to and be affected by the process of ecological adaptation is a crucial component in understanding gene expression evolution. To address these questions, we investigate the role of evolved and plastic gene expression differences in adaptation leveraging an established host plant shift in the peacock fly Tephritis conura. Using a cross-fostering design where larvae feed on either natal or alternate host plants, we uncover extensive evolved differences in gene expression between the ecotypes, strikingly in genes associated with processing of host plant chemicals. We find limited evidence for plasticity, with some indications of higher plasticity in the ancestral ecotype where the expression of three gene coexpression modules is altered when larvae are cross-fostered to the derived host plant. Interestingly, we find an enrichment of differentially expressed genes within a large, ecotype-specific inversion in the T. conura genome. This finding adds to evidence that inversions are important for enabling diversification in the face of gene flow and underscores that effects on gene expression may be key to understanding the role of inversions.

evolutionary biology↗

bioRxiv2023

The genomic landscape of adaptation to a new host plant

Adaptation to novel ecological niches is known to be rapid. However, how the loci underlying ecological divergence are coupled to traits reproductively isolating populations, ultimately enabling the formation of persistent species, remains a consequential question in speciation research. Here, we investigated the genomic differences underpinning colonization of a new niche and formation of two partly sympatric host races of Tephritis conura peacock flies. We took advantage of two independent sympatric zones west and east of the Baltic Sea, where host plant specialists using the thistle species Cirsium heterophyllum and C. oleraceum co-occur, and address what regions of the genome maintain the host races in parallel. Using genome-wide association, differentiation and divergence statistics, we identified a large, highly divergent region associated with host use among western and eastern populations. Within this region, we identified unique haplotypes associated with each host race, indicative of a large inversion, adding to the growing body of evidence that structural changes to the genome are important for adaptations to persist in the face of gene flow. We further showed strong signatures of selection in this region, especially in populations of the derived C. oleraceum specialist host race. The region also had reduced introgression, especially in western populations, while the rest of the genome showed signs of extensive gene flow. Genes within highly differentiated windows within the putative inversion were not only enriched for functions involved in host adaptation, including phenology and metabolic responses to different metabolites in the two host plants, but also enriched for gametogenesis, fertilization and embryological development, all of which suggest sequence divergence could have large consequences on reproductive isolation between the host races. In conclusion, this study suggests that structural changes in the genome may facilitate the formation of persistent host races, and ultimately speciation, in face of gene flow.

evolutionary biology↗

bioRxiv2023

Colonization of a novel host plant reduces phenotypic variation

Understanding the evolutionary potential of populations -evolvability- is key to predicting their ability to cope with novel environments. Despite growing evidence that evolvability determines the tempo and mode of adaptation, it remains unclear how adaptations to novel environments influence evolvability in turn. Here we address the interplay between adaptation and evolvability in the peacock fly Tephritis conura, which recently underwent an adaptive change in the length of female ovipositor following a host shift. By comparing evolvability in various morphological traits including female ovipositor length between ancestral and derived host races, we found that evolvability is decreased in females of the derived host race compared to the ancestral host race. We found a correlation between evolvability and divergence between populations in both sexes, indicating that the overall pattern of evolvability has not been disrupted by the host shift despite the reduction in females of the derived host race. Exploration of the pattern of phenotypic integration further revealed that the ovipositor length constitutes a module that is separated from other measured traits. These results suggest that adaptation to novel environments can affect evolvability, and that modularity helps minimizing detrimental effects that adaptations may cause to other correlated traits.

evolutionary biology↗

bioRxiv2021

Extensive transgressive gene expression in a homoploid hybrid species

Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While mis-expression in F1 hybrids is well documented, how gene expression evolves in stabilized hybrid taxa remains an open question. As gene expression evolves in a stabilizing manner, break-up of co-evolved cis- and trans-regulatory elements could lead to transgressive patterns of gene expression in hybrids. Here, we address to what extent gonad gene expression has evolved in an established and stable homoploid hybrid, the Italian sparrow (Passer italiae). Through comparison of gene expression in gonads from individuals of the two parental species (i.e., house and Spanish sparrow) to that of Italian sparrows, we find evidence for strongly transgressive expression in male Italian sparrows - 22% of testis genes exhibit expression patterns outside the range of both parent species. In contrast, Italian sparrow ovary expression was similar to that of one of the parent species, the house sparrow (Passer domesticus). Moreover, the Italian sparrow testis transcriptome is 26 times as diverged from those of the parent species as the parental transcriptomes are from each other, despite being genetically intermediate. This highlights the potential for regulation of gene expression to produce novel variation following hybridization. Genes involved in mitochondrial respiratory chain complexes and protein synthesis are enriched in the subset that is over-dominantly expressed in Italian sparrow testis, suggesting that selection on key functions have molded the hybrid Italian sparrow transcriptome.

evolutionary biology↗

bioRxiv2021

Predictors of genomic differentiation within a hybrid taxon

Hybridization is increasingly recognized as an important evolutionary force. Novel genetic methods now enable us to address how the genomes of parental species are combined to build hybrid genomes. However, we still do not know the relative importance of contingencies, genome architecture and local selection in shaping hybrid genomes. Here, we take advantage of the genetically divergent island populations of Italian sparrow on Crete, Corsica and Sicily to investigate the predictors of genomic variation within a hybrid taxon. We test if differentiation is affected by recombination rate, selection, or variation in ancestry proportion from each parent species. We find that the relationship between recombination rate and differentiation is less pronounced within hybrid lineages than between the parent species, as expected if purging of minor parent ancestry in low recombination regions reduces the variation available for differentiation. In addition, we find that differentiation between islands is correlated with differences in selection in two out of three comparisons. Patterns of within-island selection are correlated across all islands, suggesting that shared selection may mould genomic differentiation. The best predictor of strong differentiation within islands is the degree of differentiation from house sparrow, and hence loci with Spanish sparrow ancestry may vary more freely. Jointly, this suggests that constraints and selection interact in shaping the genomic landscape of differentiation in this hybrid species.

evolutionary biology↗

bioRxiv2021

Non-parallel morphological divergence following colonization of a new host plant

Divergent ecological selection may diversify conspecific populations evolving into different niches, and may lead to speciation if gene flow is ceased, e.g, due to reinforcement leading to character displacement. Adaptation to the same niche is expected to be parallel. Whether selection against maladaptive hybridization in secondary sympatry also results in parallel divergence in traits that are not directly related to the ecological niches remains an empirical challenge, although such character displacement can be decisive for if ecotypes develop into new species. Here, we use a host shift in the phytophagous peacock fly Tephritis conura, with both host races represented in two geographically separate areas East and West of the Baltic Sea to investigate convergence in morphological adaptations. We asked i) if there are consistent morphological adaptations to a host plant shift and ii) if the response to secondary sympatry with the alternate host race is parallel across contact zones. We found surprisingly low and variable, albeit significant, divergence between host races. Only one trait, the length of the female ovipositor, which serves an important function in the interaction with the hosts, was consistently different. Instead, co-existence with the other host race significantly affected the degree of morphological divergence, but the divergence was largely driven by different traits in different contact zones. Thus, local stochastic fixation or reinforcement could generate trait divergence, and additional evidence is needed to conclude whether divergence is locally adaptive.

evolutionary biology↗

bioRxiv2020

The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics

Sexually antagonistic (SA) genetic variation--in which genotypes favoured in one sex are disfavoured in the other--is predicted to be common and has been documented in several animal and plant populations, yet we currently know little about its pervasiveness among species or its population genetic basis. Recent applications of genomics in studies of SA genetic variation have highlighted considerable methodological challenges to the identification and characterisation of SA genes, raising questions about the feasibility of genomic approaches for inferring SA selection. The related fields of local adaptation and statistical genomics have previously dealt with similar challenges, and lessons from these disciplines can therefore help overcome current difficulties in applying genomics to study SA genetic variation. Here, we integrate theoretical and analytical concepts from local adaptation and statistical genomics research--including FST and FIS statistics, genome-wide association studies (GWAS), pedigree analyses, reciprocal transplant studies, and evolve-and-resequence (E&R) experiments--to evaluate methods for identifying SA genes and genome-wide signals of SA genetic variation. We begin by developing theoretical models for between-sex FST and FIS, including explicit null distributions for each statistic, and using them to critically evaluate putative signals of sex-specific selection in previously published datasets. We then highlight new statistics that address some of the limitations of FST and FIS, along with applications of more direct approaches for characterising SA genetic variation, which incorporate explicit fitness measurements. We finish by presenting practical guidelines for the validation and evolutionary analysis of candidate SA genes and discussing promising empirical systems for future work. Impact SummaryGenome sequences carry a record of the evolutionary and demographic histories of natural populations. Research over the last two decades has dramatically improved our ability to detect genomic signals of adaptation by natural selection, including several widely-used methods for identifying genes underlying local adaptation and quantitative trait variation. Yet the application of these methods to identify sexually antagonistic (SA) genes--wherein variants that are adaptive for one sex are maladaptive for the other--remains under-explored, despite the potential importance of SA selection as a mechanism for maintaining genetic variation. Indeed, several lines of evidence suggest that SA genetic variation is common within animal and plant populations, underscoring the need for analytical methods that can reliably identify SA genes and genomic signals of SA genetic variation. Here, we integrate statistics and experimental designs that were originally developed within the fields of local adaptation and statistical genomics and apply them to the context of sex-specific adaptation and SA genetic variation. First, we evaluate and extend statistical methods for identifying signals of SA variation from genome sequence data alone. We then apply these methods to re-analyse previously published datasets on allele frequency differences between sexes--a putative signal of SA selection. Second, we highlight more direct approaches for identifying SA genetic variation, which utilise experimental evolution and statistical associations between individual genetic variants and fitness. Third, we provide guidelines for the biological validation, evolutionary analysis, and interpretation of candidate SA polymorphisms. By building upon the strong methodological foundations of local adaptation and statistical genomics research, we provide a roadmap for rigorous analyses of genetic data in the context of sex-specific adaptation, thereby facilitating insights into the role and pervasiveness of SA variation in adaptive evolution.

evolutionary biology↗

bioRxiv2018

Hybridization, sex specific genomic architecture and local adaptation

While gene flow can reduce the potential for local adaptation, hybridization may conversely provide genetic variation that increases the potential for local adaptation. Hybridization may also affect adaptation through altering sexual dimorphism and sexual conflict, but this remains largely unstudied. Here, we discuss how hybridization may affect sexual dimorphism and conflict due to differential effects of hybridization on males and females, and then how this in turn may affect local adaptation. First, the lower viability of the heterogametic sex in hybrids could shift the balance in sexual conflict. Second, sex-specific inheritance of the mitochondrial genome in hybrids may lead to cyto-nuclear mismatches, for example in the form of \"mothers curse\", with potential consequences for sex-ratio and sex specific expression. Third, transgressive segregation of sexually antagonistic alleles could lead to greater sexual dimorphism in hybrid populations. These mechanisms can reduce sexual conflict and enhance intersexual niche partitioning, increasing the fitness of hybrids. Adaptive introgression of alleles reducing sexual conflict or enhancing intersexual niche partitioning may facilitate local adaptation, and could favour the colonization of novel habitats. We review these consequences of hybridization on sex differences and local adaptation, and discuss how their prevalence and importance could be tested empirically.

evolutionary biology↗

bioRxiv2018

Selection in parental species predicts hybrid evolution

While hybridization is recognized as important in evolution, its contribution to adaptation and diversification remains poorly understood. Using genomically diverged island populations of the homoploid hybrid Italian sparrow, we test predictions for phenotypic trait values and evolvability based on patterns of parental species divergence in four plumage color traits. We find associations between parental divergence and trait evolution in Italian sparrows. Fixed major QTL in species differences lead to hybrids with higher trait variation, and hence evolvability, than the parent species. Back and crown plumage show no correlation between current within-parent variability and among-parent differentiation. For these traits, Italian sparrow phenotypes are biased towards axes of high parental differentiation and show greater phenotypic novelty along axes of low current parental evolvability, as predicted when major QTL are involved in species differences. Crown color has consistently evolved back towards one parent, while back color varies among islands. We also find significant among-population diversification within the Italian sparrow. Hence, hybridization of the same parent species can generate different phenotypes. In conclusion, we find support for parental phenotypic divergence patterns reflecting divergence mechanisms, and hence such patterns can be useful in predicting how hybridization alters the potential to evolve and adapt.

evolutionary biology↗

bioRxiv2017

Genomic contingencies and beak shape variation in a hybrid species

Hybridization is increasingly recognized as a potent evolutionary force. Though additive genetic variation and novel combinations of parental genes theoretically increase the potential for hybrid species to adapt, few empirical studies have investigated the adaptive potential within a hybrid species. Here, we investigate factors promoting phenotypic divergence using genomically diverged island populations of the homoploid hybrid Italian sparrow Passer italiae from Crete, Corsica, and Sicily. We address whether genomic contingencies, adaptation to climate or diet best explain divergence in beak morphology. Populations vary significantly in beak morphology, both between and within islands of origin. Temperature seasonality best explains population divergence in beak size. Interestingly, beak shape along all significant dimensions of variation was best explained by annual precipitation, genomic composition and their interaction, suggesting a role for contingencies. Moreover, beak shape similarity to a parent species correlates with proportion of the genome inherited from that species, consistent with the presence of contingencies. In conclusion, adaptation to local conditions and genomic contingencies arising from putatively independent hybridization events jointly explain beak morphology in the Italian sparrow. Hence, hybridization may induce contingencies and restrict evolution in certain directions dependent on the genetic background.

evolutionary biology↗

bioRxiv2017

Variation and constraints in hybrid genome formation

Recent genomic investigations have revealed hybridization to be an important source of variation, the working material of natural selection1,2. Hybridization can spur adaptive radiations3, transfer adaptive variation across species boundaries4, and generate species with novel niches5. Yet, the limits to viable hybrid genome formation are poorly understood. Here we investigated to what extent hybrid genomes are free to evolve or whether they are restricted to a specific combination of parental alleles by sequencing the genomes of four isolated island populations of the homoploid hybrid Italian sparrow Passer italiae6,7. Based on 61 Italian sparrow genomes from Crete, Corsica, Sicily and Malta, and 10 genomes of each of the parent species P. domesticus and P. hispaniolensis, we report that a variety of novel and fully functional hybrid genomic combinations have arisen on the different islands, with differentiation in candidate genes for beak shape and plumage colour. There are limits to successful genome fusion, however, as certain genomic regions are invariably inherited from the same parent species. These regions are overrepresented on the Z-chromosome and harbour candidate incompatibility loci, including DNA-repair and mito-nuclear genes; loci that may drive the general reduction of introgression on sex chromosomes8. Our findings demonstrate that hybridization is a potent process for generating novel variation, but variation is limited by DNA-repair and mito-nuclear genes, which play an important role in reproductive isolation and thus contribute to speciation.

evolutionary biology↗

bioRxiv2017

Resolution of conflict between parental genomes in a hybrid species

The development of reproductive barriers against parent species is crucial during hybrid speciation, and post-zygotic isolation can be important in this process. Genetic incompatibilities that normally isolate the parent species can become sorted in hybrids to form reproductive barriers towards either parent. However, the extent to which this sorting process is systematically biased and therefore predictable in which loci are involved and which alleles are favored is largely unknown. Theoretically, reduced fitness in hybrids due to the mixing of differentiated genomes can be resolved through rapid evolution towards allelic combinations ancestral to lineage-splitting of the parent species, as these alleles have successfully coexisted in the past. However, for each locus, this effect may be influenced by its chromosomal location, function, and interactions with other loci. We use the Italian sparrow, a homoploid hybrid species that has developed post-zygotic barriers against its parent species, to investigate this prediction. We show significant bias towards fixation of the ancestral allele among 57 nuclear intragenic SNPs, particularly those with a mitochondrial function whose ancestral allele came from the same parent species as the mitochondria. Consistent with increased pleiotropy leading to stronger fitness effects, genes with more protein-protein interactions were more biased in favor of the ancestral allele. Furthermore, the number of protein-protein interactions was especially low among candidate incompatibilities still segregating within Italian sparrows, suggesting that low pleiotropy allows steep intraspecific clines in allele frequencies to form. Finally, we report evidence for pervasive epistatic interactions within one Italian sparrow population, particularly involving loci isolating the two parent species but not hybrid and parent. However there was a lack of classic incompatibilities and no admixture linkage disequilibrium. This suggests that parental genome admixture can continue to constrain evolution and prevent genome stabilization long after incompatibilities have been purged.

evolutionary biology↗