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 aging, 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 aging in each sex.

Keywords: RNA-seq; aging; experimental evolution; life history evolution; longevity; sex bias.

Fig. 1.

The unfolding of sex-specific (females: red; males: blue) divergence in lifespan between the E and L lines over time (mated individuals). Solid lines represent the fitted function Y = 1 + a(1 − b^X). Female lifespan evolved more rapidly (b: t = 2.46, P = 0.030) and has reached a greater divergence (a: t = 2.83, P = 0.015) relative to male lifespan divergence. Adult life span was assayed by allowing newly enclosed males and females to mate, and then separating the sexes into petri dishes where life span was monitored by daily spot checks (see Tucić 1996, 1998 for details).

Fig. 2.

Repeatability estimates (with 95% bootstrap CI) of gene expression across the four replicate E and the four replicate L lines, for each sex and tissue.

Fig. 3.

Principle component analysis of gene expression in the (a) reproductive and (b) somatic tissues of the E and L lines. The axes show the first and second principle components with the % of variance explained by each.

Fig. 4.

(a and b) Numbers of DE genes (q < 0.05, abs. logFC > 1) between the (E)arly and (L)ate EE regimes in each sex. (c) Overlap of genes significant in each tissue category and sex (Abd = abdomen; HT = head and thorax; F = females; M = males).

Fig. 5.

(a and b) Numbers of sex-biased genes in the E and L regimes. (c–f) Average expression of DE female-, male-, and un-biased genes in each sex. Significant median difference between the regimes: ***P < 0.001, *P < 0.05.