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Abstract
It is the differences between sperm and eggs that fundamentally underpin the differences between the sexes within reproduction. For males, it is theorized that widespread sperm competition leads to selection for investment in sperm numbers, achieved by minimizing sperm size within limited resources for spermatogenesis in the testis. Here, we empirically examine how sperm competition shapes sperm size, after more than 77 generations of experimental selection of replicate lines under either high or low sperm competition intensities in the promiscuous flour beetle Tribolium castaneum. After this experimental evolution, populations had diverged significantly in their sperm competitiveness, with sperm in ejaculates from males evolving under high sperm competition intensities gaining 20% greater paternity than sperm in ejaculates from males that had evolved under low sperm competition intensity. Males did not change their relative investment into sperm production following this experimental evolution, showing no difference in testis sizes between high and low intensity regimes. However, the more competitive males from high sperm competition intensity regimes had evolved significantly longer sperm and, across six independently selected lines, there was a significant association between the degree of divergence in sperm length and average sperm competitiveness. To determine whether such sperm elongation is costly, we used dietary restriction experiments, and revealed that protein‐restricted males produced significantly shorter sperm. Our findings therefore demonstrate that sperm competition intensity can exert positive directional selection on sperm size, despite this being a costly reproductive trait.
Highlights
Our understanding of the evolution of sperm form and function has its roots in anisogamy theory, where numerical competition for fertilizations was proposed to shape the fundamental phenotype of a male gamete that was produced in vast numbers, achieved via minimizing sperm size and increasing testicular investment (Parker et al 1972, 1997; Parker 1982; Lessells et al 2009; Parker and Pizzari 2010)
In parallel with the divergence in sperm competitiveness, we found significant differences in sperm length under strong versus weak selection from sperm competition, and both increases and decreases relative to the ancestral population average (Fig. 2A and B)
Given similar investment into spermatogenesis, the divergence in sperm competitiveness and sperm length between our selection regimes indicates that more intense sperm competition can select for qualitative improvements within individual sperm cell phenotypes, and not necessarily a basic drive to increase sperm numbers
Summary
Our understanding of the evolution of sperm form and function has its roots in anisogamy theory, where numerical competition for fertilizations was proposed to shape the fundamental phenotype of a male gamete that was produced in vast numbers, achieved via minimizing sperm size and increasing testicular investment (Parker et al 1972, 1997; Parker 1982; Lessells et al 2009; Parker and Pizzari 2010). Spermatozoa are the most morphologically diverse eukaryotic cell types known (Pitnick et al 2009a); even sperm size alone varies more than 8000-fold, from the diminutive gametes of the male braconid parasitoid wasp Cotesia congregata (7 μm; Uzbekov et al 2017) to the giant sperm of Drosophila bifurca (58,290 μm; Pitnick et al 1995) Most of this profound variation remains unexplained, but the diversity in form and function suggests that the selective forces shaping sperm form and function are more complex than a basic drive to win fertilization competitions by maximizing sperm number and minimizing sperm size
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