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Immonen, E.

Publications and source records attributed to Immonen, E..

7 recordsLinked to original sources

Experimental evolution unveils a role for structural variants and sex-specificity in the genetic architecture of lifespan

Insights into the genetic basis of lifespan evolution can link evolutionary theory with an understanding of health, disease and adaptation. We leverage the power of >200 generations of experimental evolution in a seed beetle to unveil the genomic architecture of lifespan evolution. Replicated populations evolved under regimes favoring either a short or long life, resulting in a near doubling of lifespan. Whole genome re-sequencing revealed that short- and long-lived lines were strongly differentiated (global FST = 0.41) and more than 700 genes showed consistent signs of divergent selection. Remarkably, short- and long-lived lines were consistently divergent in a large number of regions harboring copy-number variants (CNVs), involving >600 genes. The evolution of a long life involved many distinct biological processes, such as DNA fidelity, mitotic integrity, reproduction, metabolism, immunity and stress response. A pedigree-based genome scan for quantitative trait loci (QTLs) uncovered several QTLs with large effects on lifespan, but the genetic basis of a long life was dominated by a very large number of regions with medium and small effects. The genome-wide spatial association with QTL effects was, if anything, stronger for CNVs than for sequence variants. The genetic effects of QTLs on lifespan were positively correlated overall between the sexes, but four regions showed pronounced sex-differences. Our results show that structural variants play a significant role in the evolution of an extended lifespan and the highly polygenic genomic architecture is to some extent sex-specific, consistent with differences in physiology and life history tradeoffs between the sexes.

evolutionary biology↗

Uniform annotation framework reveals genome size and LINE/LTR retrotransposons as predictors of gene family expansion across Coleoptera

Gene family evolution - the turnover of duplicated homologous genes - shapes genome architecture and fuels phenotypic innovation. Repetitive elements (REs) facilitate gene duplication and genome expansion, yet whether variation in repeat abundance and genome size (GS) scales with gene family evolution across species remains unclear. Coleoptera provides a well-suited system for examining these dynamics because of its major ecological diversification and extensive genome size variation. Comparative tests of these relationships are however hindered by heterogenous genome annotations that distort gene counts and orthogroup assignments. We first evaluate how repeat- and gene-annotation strategies influence gene- and orthogroup-detection across beetle genomes. We then apply unified re-annotations of both to identify rapidly evolving gene families and test whether GS and repeat content covary with gene family size evolution. Nearly 500 orthogroups are rapidly evolving in Coleoptera, many of which are linked to ecologically crucial functions such as chemosensory perception and detoxification. GS and RE abundance are correlated, and on average scale positively with gene family sizes. LINE and DNA transposable elements commonly flank rapidly expanding gene families, but with pronounced species-specific variation. Together, these findings position genome architecture and repeat dynamics as fundamental determinants of gene family evolvability.

evolutionary biology↗

From constraint to opportunity: Relaxing sexual antagonism reveals adaptive potential maintained by balancing selection

Despite ongoing selection, genetic variation in fitness-related traits often persists. Balancing selection can maintain polymorphisms through genetic trade-offs, including those between the sexes. Sexually antagonistic (SA) selection is challenging to detect at the genomic level and its broader evolutionary importance, especially for complex traits, remains unclear. To investigate this, we conducted an evolve-and-resequence experiment in Callosobruchus maculatus, manipulating the strength of SA trade-offs over body size and tracking genome-wide responses. When selection simultaneously favored larger females and smaller males, allele frequency changes were constrained and genome-wide divergence remained limited. In contrast, relaxing SA trade-offs by selecting on only one sex led to large, repeatable allele frequency shifts. These loci also showed signatures of long-term balancing selection in the ancestral population. Together, our results demonstrate that SA trade-offs can act both as a constraint, limiting sex-specific responses under antagonistic selection pressures, but also as a source of adaptive potential once antagonism is relaxed.

evolutionary biology↗

Sex-biased gene expression under sexually antagonistic and sex-limited selection

Sex differences in gene expression are ubiquitous, evolve quickly, and are expected to underlie phenotypic sexual dimorphism. Despite long-standing interest, the impact of sex- specific selection on the transcriptome remains poorly understood. Here, we test fundamental questions on the role of constraints on gene expression evolution arising from the mode of selection and genetic architecture. We also test the relationship between sex-biased expression and evolved sexual dimorphism (SD). We assess these using body size selection lines in the seed beetle, Callosobruchus maculatus, that have evolved variation in SD in response to either sex-limited (SL) or sexually antagonistic (SA). We find that sex differences in the phenotypic responses and expression changes are generally well aligned. SL selection, despite a phenotypic response similar to SA selection in males, but not in females, resulted in a more extensive expression differentiation and increase of sex-biased expression than SA selection. These patterns show that SA selection imposes a transcriptomic constraint and is not required for sex-bias to evolve. Sex-biased transcripts show lower cross-sex correlations in expression changes than unbiased transcripts, suggesting greater sex differences in their underlying genetic architecture. Although male-biased transcripts are disproportionately affected when selection targeted males, we find no support for a transcriptome-wide association between sex-bias and SD. In the light of these unique experimental insights into how sex-specific selection on size changes adult transcription, our findings have important implications for inferring selection history and mode from patterns of sex-biased gene expression in natural populations.

evolutionary biology↗

Y-linked copy number polymorphism of target of rapamycin(TOR) is associated with sexual size dimorphism in seed beetles

The Y chromosome is theorized to facilitate evolution of sexual dimorphism by accumulating sexually antagonistic loci, but empirical support is scarce. Due to the lack of recombination Y chromosomes are prone to degenerative processes, which poses a constraint on their adaptive potential. Yet, in the seed beetle Callosobruchus maculatus segregating Y linked variation affects male body size and thereby sexual size dimorphism (SSD). Here we assemble C. maculatus sex chromosome sequences and identify molecular differences associated with Y-linked SSD variation. The assembled Y chromosome is largely euchromatic and contains over 400 genes, many of which are ampliconic with a mixed autosomal and X chromosome ancestry. Functional annotation suggests that the Y chromosome plays important roles in males beyond primary reproductive functions. Crucially, we find that, besides an autosomal copy of the gene target of rapamycin (TOR), males carry an additional TOR copy on the Y chromosome. TOR is a conserved regulator of growth across taxa, and our results suggest that a Y-linked TOR provides a male specific opportunity to alter body size. A comparison of Y haplotypes associated with male size difference uncovers a copy number variation for TOR, where the haplotype associated with decreased male size, and thereby increased sexual dimorphism, has two additional TOR copies. This suggests that sexual conflict over growth has been mitigated by autosome to Y translocation of TOR followed by gene duplications. Our results reveal that despite of suppressed recombination, the Y chromosome can harbour adaptive potential as a male-limited supergene.

evolutionary biology↗

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

BackgroundSexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex-differences in immunity as well as associated host-pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. ResultsWe demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex-differences in the expression of genes in the pro-phenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females have evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. ConclusionsOur study provides insights into the links between sexual conflict and sexual dimorphism in immunity at the molecular and phenotypic level and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host-pathogen dynamics in sexually reproducing organisms.

evolutionary biology↗

Female resource limitation does not make the opportunity for selection more female biased.

Environmental and physiological conditions affect how individual variation is expressed and translated into variance in fitness, the opportunity for natural selection. Competition for limiting resources can magnify variance in fitness and therefore selection, while abundance of resources should reduce it. But even in a common environment the strength of selection can be expected to differ across the sexes, as their fitness is often limited by different resources. Indeed most taxa show a greater opportunity for selection in males than in females, a bias often ascribed to intense competition among males for access to mating partners. This sex-bias could reverberate on many aspects of evolution, from speed of adaptation to genome evolution. It is unclear however, whether the sex-bias in opportunity for selection is robust to variations in environment or physiological condition that limit sex-specific resources. Here we test this in the model species C. maculatus by comparing female and male variance in relative fitness (opportunity for selection) under mate competition (i) with and without limitation of quality oviposition sites, and (ii) under delayed age at oviposition. Decreasing the abundance of the resource key to females or increasing their reproductive age was indeed challenging as shown by a reduction in mean fitness, however variance in fitness remained male-biased across the three treatments, with even an increased male-bias when females were limited by oviposition sites. This suggests that males remain the more variable sex independent of context, and that the opportunity for selection through males is indirectly affected by female-specific resource limitation.

evolutionary biology↗