Experimental Life History Evolution Results in Sex-specific Evolution of Gene Expression in Seed Beetles

Abstract

The patterns of reproductive timing and senescence vary within and across species owing to differences in reproductive strategies, but our understanding of the molecular underpinnings of such variation is incomplete. This is perhaps particularly true for sex differences. We investigated the evolution of sex specific gene expression associated with life history divergence in replicated populations of the seed beetle Acanthoscelides obtectus, experimentally evolving under (E)arly or (L)ate life reproduction for >200 generations which has resulted in strongly divergent life histories. We detected 1,646 genes that were differentially expressed in E and L lines, consistent with a highly polygenic basis of life history evolution. Only 30% of differentially expressed genes were similarly affected in males and females. The evolution of long life was associated with significantly reduced sex differences in expression, especially in non-reproductive tissues. The expression differences were overall more pronounced in females, in accordance with their greater phenotypic divergence in lifespan. Functional enrichment analysis revealed differences between E and L beetles in gene categories previously implicated in ageing, such as mitochondrial function and defense response. The results show that divergent life history evolution can be associated with profound changes in gene expression that alter the transcriptome in a sex-specific way, highlighting the importance of understanding the mechanisms of ageing in each sex.

A chromosome-level assembly of the seed beetle Callosobruchus maculatus genome with annotation of its repetitive elements

“…In closing, we note that seed beetles may also provide future insights into the possible role of repeats in adaptive evolution, as genome size is associated with organismal function ( Arnqvist et al . 2015 ; Boman and Arnqvist 2023 ) and because transcripts related to DNA-mediated transposition show differential abundance in experimental life history evolution lines in seed beetles ( Immonen et al . 2023 ).…”

Comparative Genomic Analysis of the Pattern of Evolution of Male and Female Reproductive Proteins in Seed Beetles

“…We employed the published genome assemblies of C. maculatus ( Sayadi et al 2019 ) and A. obtectus ( Immonen et al 2023 ; European Nucleotide Archive, accessions PRJEB30475 and PRJEB51445, respectively). Both assemblies are well-annotated high-quality assemblies based on long-read PacBio sequencing data.…”

“…A documentation of conspecific sperm precedence in seed beetles also implies that reproductive proteins may be involved in incipient speciation ( Rugman-Jones and Eady 2007 ). Here, we sequenced and de novo assembled the genomes of Callosobruchus chinensis and Callosobruchus analis which then enabled the first comparative genomic analyses of SFP and FRP orthologs in four species of seed beetles, given that genome assemblies are already available for two species ( C. maculatus and Acanthoscelides obtectus ) ( Sayadi et al 2019 ; Immonen et al 2023 ; Arnqvist et al 2024 ).…”