Larval social cues influence testicular investment in an insect

Abstract

Socio-sexual environment can have critical impacts on reproduction and survival of animals. Consequently, they need to prepare themselves by allocating more resources to competitive traits that give them advantages in the particular social setting they have been perceiving. Evidence shows that a male usually raises his investment in sperm after he detects the current or future increase of sperm competition because relative sperm numbers can determine his paternity share. This leads to the wide use of testis size as an index of the sperm competition level, yet testis size does not always reflect sperm production. To date, it is not clear whether male animals fine-tune their resource allocation to sperm production and other traits as a response to social cues during their growth and development. Using a polygamous insect Ephestia kuehniella, we tested whether and how larval social environment affected sperm production, testis size and body weight. We exposed the male larvae to different juvenile socio-sexual cues and measured these traits. We demonstrate that regardless of sex ratio, group-reared males produced more eupyrenes (fertile and nucleate sperm) but smaller testes than singly-reared ones, and that body weight and apyrene (infertile and anucleate sperm) numbers remained the same across treatments. We conclude that the presence of larval social, but not sexual cues, is responsible for the increase of eupyrene production and decrease of testis size. We suggest that male larvae increase investment in fertile sperm cells and reduce investment in other testicular tissues in the presence of conspecific juvenile cues.

Pupal Cues Increase Sperm Production but Not Testis Size in an Insect

“…For example, male animals may invest more in sperm after they detect the presence of rivals to gain an advantage in sperm competition [2,[4][5][6][7][8][9][10]. In insects, males fine-tune their sperm investment in response to sex specific cues experienced during the adult stage [10][11][12][13][14][15][16] or non-sex specific cues during the Insects 2021, 12, 679 2 of 9 larval stage [17][18][19][20][21]. Although insect pupae do not feed and crawl, they can communicate with each other using species-specific acoustic [22][23][24][25][26][27][28][29] or chemical cues [30][31][32][33][34].…”

“…For example, with the increase in larval density, testis size increases in some species, suggesting an increase of sperm production (sperm were not counted though) [17,39,40]. In a study where testis size is measured and sperm are counted [19], the male larvae exposed to larval cues, regardless of sex, produce smaller testes but more fertile sperm. These discoveries suggest that in response to their social environment, male larvae are able to dedicate varying portions of testis volumes to spermatogenesis and other functions [41], resulting in potential trade-offs between traits of different functions [19,[42][43][44].…”

“…In a study where testis size is measured and sperm are counted [19], the male larvae exposed to larval cues, regardless of sex, produce smaller testes but more fertile sperm. These discoveries suggest that in response to their social environment, male larvae are able to dedicate varying portions of testis volumes to spermatogenesis and other functions [41], resulting in potential trade-offs between traits of different functions [19,[42][43][44]. However, there is no report that insects can alter their testis size in response to the socio-sexual environment experienced at the adult stage.…”

“…Adults of this species do not feed so they acquire all resources via larval feeding [49,50]. The pupal stage lasts about eight days [19,51,52], during which time, females emit sex pheromones [36]. Like most lepidopterans [53], E. kuehniella males produce two types of sperm, larger nucleated eupyrenes during the larval and pupal stages, and smaller anucleated apyrenes during the pupal stage [54].…”

“…The apyrene-to-eupyrene ratio remains consistent under food shortage during the larval stage [61] or environmental stress during the larval [62] and pupal stages [63]. However, E. kuehniella males increase the ratio after detecting rival cues during the adult stage [10] or reduce it following exposure to larval cues during the larval stage [19]. So far, it is still unclear whether the socio-sexual environment during the pupal stage affects the sperm production ratio.…”