Differential gene regulation in selected lines for high and low sperm production in male guppies

Abstract

In species where females mate with more than one male during the same reproductive event, males typically increase the number of sperm produced to boost their fertilization share. Sperm is not limitless, however, and theory predicts that their production will come at the cost of other fitness-related traits, such as body growth or immunocompetence, although these evolutionary trade-offs are notoriously difficult to highlight. To this end, we combined artificial selection for sperm production with a transcriptome analysis using Poecilia reticulata, a fish characterized by intense sperm competition in which the number of sperm transferred during mating is the most important predictor of fertilization success, yet sperm production is highly variable among males. We compared the brain and testes transcriptome in male guppies of lines artificially selected for high and low sperm production by identifying pivotal differentially expressed gene sets that may regulate spermatogenesis and immune function in this species. Despite the small differences in single genes' expression, gene set enrichment analysis showed coordinated gene expression differences associated with several pathways differentially regulated in the two selection lines. High sperm production males showed an upregulation of pathways related to immunosuppression and development of spermatozoa indicating a possible immunological cost of sperm production.

Molecular insights into post‐mating immune response in a fish with internal fertilization

“…For example, it has been demonstrated that immune‐challenged individuals exhibit reduced reproductive success and that increased investment in reproduction often results in decreased immunocompetence (Adamo, Jensen, & Younger, 2001; Fedorka, Zuk, & Mousseau, 2004; Rolff & Siva‐Jothy, 2002; Schmid‐Hempel, 2003). This trade‐off between immunity and reproduction is also reported specifically for the production of gametes (Devigili, Belluomo, Locatello, Rasotto, & Pilastro, 2017; McNamara, Lieshout, & Simmons, 2014; Radhakrishnan & Fedorka, 2012; Cattelan, Vidotto, Devigili, Pilastro, & Grapputo 2020). However, it is now clear that immunity and reproduction are linked beyond these trade‐offs, as there is evidence, in a wide taxonomic range of species, of a link between immunity and competitive fertilization success, that is when sperm from two or more males compete to fertilize the same set of eggs (Lawniczak et al, 2007; Morrow & Innocenti, 2012).…”

Sperm production is negatively associated with muscle and sperm telomere length in a species subjected to strong sperm competition

“…We established a panel of four non-VCN candidate genes on four different linkage groups (LG) of the guppy genome: the MC1R itself on LG3, the intermediate filament protein ON3-like on LG2, an uncharacterized protein on LG1 and the β actin on LG 8. The intermediate filament protein and the uncharacterized protein showed similar expression in high and low sperm guppy selected lines (Cattelan, Vidotto, et al, 2020), while the β actin is usually used as a housekeeping gene in gene expression analysis (e.g., Zhang et al, 2023). Locus ID, primers sequences and RT-qPCR profiles are reported in Table S1.…”