Juvenile socio‐sexual experience determines lifetime sperm expenditure and adult survival in a polygamous moth, Ephestia kuehniella

Abstract

Male animals often adjust their sperm investment in response to sperm competition environment. To date, only a few studies have investigated how juvenile sociosexual settings affect sperm production before adulthood and sperm allocation during the first mating. Yet, it is unclear whether juvenile sociosexual experience (1) determines lifetime sperm production and allocation in any animal species; (2) alters the eupyrene : apyrene sperm ratio in lifetime ejaculates of any lepidopteran insects, and (3) influences lifetime ejaculation patterns, number of matings and adult longevity. Here we used a polygamous moth, Ephestia kuehniella , to address these questions. Upon male adult emergence from juveniles reared at different density and sex ratio, we paired each male with a virgin female daily until his death. We dissected each mated female to count the sperm transferred and recorded male longevity and lifetime number of matings. We demonstrate for the first time that males ejaculated significantly more eupyrenes and apyrenes in their lifetime after their young were exposed to juvenile rivals. Adult moths continued to produce eupyrene sperm, contradicting the previous predictions for lepidopterans. The eupyrene : apyrene ratio in the lifetime ejaculates remained unchanged in all treatments, suggesting that the sperm ratio is critical for reproductive success. Male juvenile exposure to other juveniles regardless of sex ratio caused significantly shorter adult longevity and faster decline in sperm ejaculation over successive matings. However, males from all treatments achieved similar number of matings in their lifetime. This study provides insight into adaptive resource allocation by males in response to juvenile sociosexual environment.

Male larval experience of cues from adult rivals alters lifetime sperm investment patterns in a sperm heteromorphic moth, Ephestia kuehniella

“…For each treatment, lines between boxes with "*" and "ns" indicate significantly different (P < 0.05) and not significantly different (P > 0.05), respectively. (Liu et al, 2022) and in lifetime ejaculates (Liu et al, 2023) in E. kuehniella. However, our current study indicates that the higher sperm production during the juvenile stage in response to adult males (Fig.…”

“…5). These findings suggest that (1) the number of spermatogonia for producing eupyrenes may be limited (Witalis & Godula, 1993; Jarrige et al, 2015;Mari et al, 2018) so that the adults cannot manufacture more eupyrenes if their juveniles have used most or all of them, and (2) the number of cells for producing apyrenes may be less limited (Silberglied et al, 1984;Cook & Gage, 1995;Liu et al, 2023), allowing adults to produce more apyrene throughout their life regardless of their larval experience. Production of more apyrenes throughout lifetime may be important to gain advantages in sperm competition and fertilization success (Cook & Wedell, 1999;Holman & Snook, 2008;Wedell et al, 2009;Sakai et al, 2019;Hague et al, 2021).…”

“…3). The lack of response to adult cues by younger larvae may be attributed to the fact that testes start forming their shape only when the larvae reach the fourth instar (about 15 d old) (Liu et al, 2022(Liu et al, , 2023, allowing them to adjust their sperm production from this stage on. The shorter mating latency induced by adult male cues implies that intramale competition risk also reduces mate selectivity by males.…”

“…, 1984; Cook & Gage, 1995; Liu et al. , 2023), allowing adults to produce more apyrene throughout their life regardless of their larval experience. Production of more apyrenes throughout lifetime may be important to gain advantages in sperm competition and fertilization success (Cook & Wedell, 1999; Holman & Snook, 2008; Wedell et al.…”

Effects of juvenile situational experience on behavioral development of Brandt's vole (Lasiopodomys brandtii): From cognition to psychology

“…Environmental factors and the nature of these experiences can result in both positive and adverse outcomes (Baroncelli et al., 2010). For instance, studies have indicated that social environments during adolescence influence reproductive aspects in the Mediterranean flour moth ( Ephestia kuehniella ; Liu et al., 2022), and adverse experiences have been linked to altered emotional reactivity in rhesus macaques ( Macaca mulatta ; Howell et al., 2014). Understanding the underlying mechanisms of these experiences is crucial for developing interventions that promote healthy development and overall well‐being in animals.…”