Sex-specific variation in thermal sensitivity has multiple negative effects on reproductive trait performance

Understanding how increasing temperatures influence ectotherm population
growth rate is necessary for predicting population persistence. Population
growth rate depends on the thermal performance of multiple life-history
traits that have different thermal sensitivities. Reproductive traits are
considered more thermally sensitive than other life-history traits, such
as survival and development rate. Moreover, thermal sensitivity of
reproductive traits can be sex-specific, which may differentially affect
population growth. However, research concurrently assessing the
sex-specific influence of heat stress on multiple reproductive traits is
limited. We investigated the effect of heat stress on pupal survival and
reproductive traits in both sexes to determine sex-specific thermal
sensitivity and reproductive performance. Individuals of the butterfly
Pieris napi were reared at either 22°C or 29°C throughout larval and pupal
stages. The latter temperature reflects fastest development rate in this
population, influencing generation time, a common population growth rate
metric. We recorded pupal survival and adult body weight in both sexes.
After eclosion, males and females from both treatments were allowed to
interact, and mating success, copulation duration, egg production,
fertility and male sterility recovery were measured. A subset of mated
females was dissected to assess the number and length of fertilising
eupyrene and non-fertilising apyrene sperm transferred by males of each
treatment. While elevated temperatures reduced pupal survival and resulted
in smaller body weights in both sexes, more substantial sex-specific
effects on reproductive traits were observed. Mating success was reduced
in heat-treated females but not males. In contrast, female egg production
and fertility was unaffected by thermal treatment while heat-stressed
males, despite having longer copulation durations, exhibited near-complete
sterility. Male heat-induced sterility was mediated by a disruption to
both eupyrene and apyrene sperm production or transfer. Male remating did
not recover fertility, suggesting continued negative effects on sperm
production. Our results highlight how increasing temperatures affect
reproduction, illustrating that temperatures generating optimal
performance for non-reproductive traits, like development rate, can
negatively and differentially impact sex-specific reproductive fitness.
These negative reproductive consequences may impact population
persistence, highlighting the necessity to incorporate these findings into
future advanced models predicting species’ responses to climate warming.