Abstract
When females mate with multiple partners in a reproductive cycle, the relative number of competing sperm from rival males is often the most critical factor in determining paternity. Gamete production is directly related to testis size in most species, and is associated with both mating behavior and perceived risk of competition. Deer mice, Peromyscus maniculatus, are naturally promiscuous and males invest significantly more in sperm production than males of P. polionotus, their monogamous sister‐species. Here, we show that the larger testes in P. maniculatus are retained after decades of enforced monogamy in captivity. While these results suggest that differences in sperm production between species with divergent evolutionary histories can be maintained in captivity, we also show that the early rearing environment of males can strongly influence their testis size as adults. Using a second‐generation hybrid population to increase variation within the population, we show that males reared in litters with more brothers develop larger testes as adults. Importantly, this difference in testis size is also associated with increased fertility. Together, our findings suggest that sperm production may be both broadly shaped by natural selection over evolutionary timescales and also finely tuned during early development.
Highlights
Peromyscus rodents exhibit striking variation in testicular, ejaculate and sperm traits across species (Linzey & Layne, 1969, 1974), which are associated with differences in mating strategy (Bedford & Hoekstra, 2015; Turner et al, 2010). This trend is perhaps best exemplified by two sister-species, the deer mouse (P. maniculatus) and the oldfield mouse (P. polionotus)
We found no effect of male age on male fertility (LM: N = 85, p = 0.69) or on testis size (LMM: N = 300, p = 0.70)
Our results suggest that both evolutionary history and social cues during development can have an important effect on investment in sperm production in Peromyscus mice
Summary
In systems in which females mate multiply, the competition among sperm from different males to fertilize the available ova can be intense and drive the evolution of male reproductive traits (Parker, 1970). Peromyscus rodents exhibit striking variation in testicular, ejaculate and sperm traits across species (Linzey & Layne, 1969, 1974), which are associated with differences in mating strategy (Bedford & Hoekstra, 2015; Turner et al, 2010). This trend is perhaps best exemplified by two sister-species, the deer mouse (P. maniculatus) and the oldfield mouse (P. polionotus). Consistent with the well-documented relationship between relative testis size and level of sperm competition in rodents (Ramm, Parker, & Stockley, 2005), wild-caught P. maniculatus have testes roughly twice as large as those observed in P. polionotus males (Linzey & Layne, 1969). Using a second-generation hybrid intercross of these two Peromyscus species to generate a greater range of reproductive phenotypes (Bendesky et al, 2017; Fisher, Jacobs-Palmer, Lassance, & Hoekstra, 2016) and to break up co- adapted gene complexes (West-Eberhard, 2003), we examine whether the social composition of the early developmental environment affects sperm production in adults and impacts reproductive potential
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