Sibling rivalry: Males with more brothers develop larger testes

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.

Exposure to male-dominated environments during development influences sperm sex ratios at sexual maturity

“…; Fisher et al. ). Adding to this, our current investigation suggests that differences in testosterone levels of individuals exposed to different postmaternal social regimes may also lead to variation in sperm sex ratios.…”

“…; Fisher et al. ). For example, male house mice that mature under a perceived risk of male–male competition invest more in growth (André et al.…”

Increased sperm production linked to competition in the maternal social environment

“…Finally, since exposure to androgens in utero from male siblings can influence sperm production traits [ 17 ], we tested if the number of sons per litter or litter sex ratio differed according to treatment group. However, there was no difference between treatment groups in the number of sons per litter (mean ± s.e.…”

“…Other studies, involving more subtle variation in androgen exposure have shown different outcomes. For example, it is well known that the development of male rodents is influenced by their intra-uterine position; that is, male foetuses positioned between two brothers ultimately develop larger testes as a result of higher prenatal androgen exposure [ 47 , 48 ], and there is evidence that males with more male siblings in utero also have increased fertility [ 17 ]. While we cannot exclude the possibility of passive exposure to androgens from siblings in utero as an explanation for our results, it seems unlikely.…”

Evolutionary rates of testes-expressed genes differ in monogamous and promiscuousPeromyscusspecies

“…Faster, more viable sperm and higher sperm counts have been shown to yield an increased chance of fertilization and thus a fitness advantage in promiscuous species (Pizzari 2006). Indeed, promiscuous males often possess larger testes and produce more abundant and more competitive sperm than monogamous males, even in the case of recently diverged species (Heske and Ostfeld 1990;Shuster 2009;Firman and Simmons 2010a;Claw et al 2018;Fisher et al 2018). However, the genetic basis of morphological and physiological differences related to differences in mating system remain largely unexplored.…”