Sublethal heat reduces overall reproductive investment and male allocation in a simultaneously hermaphroditic snail species.

The exposure to sublethally high temperature reduces reproductive performance in diverse organisms. Although this effect has been particularly emphasized for males or male reproductive functioning, it remains largely unknown whether the effect of heat on fertility is sex-specific. Here we examined the impact of sublethally high temperature on male and female functions in a simultaneously hermaphroditic snail species, Lymnaea stagnalis. Examining hermaphrodites is useful to evaluate the sex-specific impacts of heat exposure, since they possess male and female functions within a single individual, sharing genetic and environmental factors. Moreover, previously developed sex allocation theory allows us to compare the differential performance of sex functions. In this study, we exposed snails to 20°C (control), 24°C and 28°C for 14 days and assessed their egg and sperm production, sperm transfer, mating behaviour and growth. Both types of gamete production were significantly reduced by higher temperature, leading to an overall reduction of reproductive investment. By quantifying sex allocation, we furthermore revealed that the heat-stressed snails reduced the relative investment in their male function. This study illustrates that examining simultaneous hermaphrodites can provide significant insights for the impact of heat, and the proximate mechanism, on reproduction in diverse organisms.

Male reproductive suppression: not a social affair.

In the animal kingdom there are countless strategies via which males optimize their reproductive success when faced with male-male competition. These male strategies typically fall into two main categories: pre- and post-copulatory competition. Within these 2 categories, a set of behaviors, referred to as reproductive suppression, is known to cause inhibition of reproductive physiology and/or reproductive behavior in an otherwise fertile individual. What becomes evident when considering examples of reproductive suppression is that these strategies conventionally encompass reproductive interference strategies that occur between members of a hierarchical social group. However, mechanisms aimed at impairing a competitor's reproductive output are also present in non-social animals. Yet, current thinking emphasizes the importance of sociality as the primary driving force of reproductive suppression. Therefore, the question arises as to whether there is an actual difference between reproductive suppression strategies in social animals and equivalent pre-copulatory competition strategies in non-social animals. In this perspective paper we explore a broad taxonomic range of species whose individuals do not repeatedly interact with the same individuals in networks and yet, depress the fitness of rivals. Examples like alteration of male reproductive physiology, female mimicry, rival spermatophore destruction, and cementing the rival's genital region in non-social animals, highlight that male pre-copulatory reproductive suppression and male pre-copulatory competition overlap. Finally, we highlight that a distinction between male reproductive interference in animals with and without a social hierarchy might obscure important similarities and does not help to elucidate why different proximate mechanisms evolved. We therefore emphasize that male reproductive suppression need not be restricted to social animals.

Alternative delivery of male accessory gland products.

To increase fertilization success, males transfer accessory gland products (Acps). Several species have evolved unconventional Acps transfer modes, meaning that Acps are transferred separately from the sperm. By surveying the sperm-free Acps transfer cases, we show that these animals have evolved a common strategy to deliver Acps: they all inject Acps directly through the partner's body wall into the hemolymph. Our review of this mode of Acps transfer reveals another striking similarity: they all transfer sperm in packages or via the skin, which may leave little room for Acps transfer via the conventional route in seminal fluid. We synthesise the knowledge about the function, and the effects in the recipients, of the Acps found in the widely diverse taxa (including earthworms, sea slugs, terrestrial snails, scorpions and salamanders) that inject these substances. Despite the clearly independent evolution of the injection devices, these animals have evolved a common alternative strategy to get their partners to accept and/or use their sperm. Most importantly, the evolution of the injection devices for the delivery of Acps highlights how the latter are pivotal for male reproductive success and, hence, strongly influence sexual selection.

Male-male competition leads to less abundant but more attractive sperm.

Males employ complex strategies to optimize their reproductive success when faced with male-male competition; for instance, they can adjust the ejaculate characteristics. In copulating species, a male may also strategically adjust his ejaculate expenditure according to female quality. Quantifying the relative contribution of ejaculate plasticity in male reproductive success is often difficult, especially when females exert postcopulatory cryptic choice. One way to quantify the functional significance of ejaculate plasticity is offered by mating systems in which the reproductive partners do not meet each other during insemination. In the collembolan Orchesella cincta, males deposit their ejaculates (spermatophores) irrespective of the presence of females. We tested whether Orchesella males adjust spermatophore number when exposed to the presence of another male and whether changes in spermatophore production influence female choice. We found that Orchesella males display plasticity in spermatophore allocation. Males decreased the spermatophore number when exposed to a rival male. Moreover, females preferentially took up spermatophores of males that were exposed to a competitor. The reduction in spermatophore number suggests, besides an adaptive response to the risk of ejaculate removal by rival males, an optimization strategy owing to the costs of more attractive spermatophores.

Effects of exposure to short-term heat stress on male reproductive fitness in a soil arthropod.

Ambient temperature is a key environmental factor influencing a variety of aspects of the ecology and evolution of ectotherms. Reproductive traits have been suggested to be more sensitive to thermal stress than other life history traits. This study investigated the direct and indirect effects of heat shock on male reproductive success in the widespread springtail Orchesella cincta. Male springtails were exposed to four temperature treatments: heat hardening (35.2°C for 1h), heat shock (37.2°C for 1h), heat hardening+heat shock (35.2°C for 1h, followed 15h later by 37.2°C for 1h), and control (20°C). The heat shock gene Hsp70 showed high expression in all the heat treatments, indicating that the treatments indeed induced thermal stress. Significant mortality was only found in the treatment with heat shock, both with and without heat hardening. A direct effect of heat treatment was found on time to first reproduction, which was significantly longer after heat shock (with or without heat hardening) than in the control treatment. There was no difference among treatments in the number of spermatophores produced in the first reproductive instar. Heat treatment also had indirect effects on male reproductive success. Females chose significantly more spermatophores from control males than from males that received heat shock, heat hardening or both. A high percentage of spermatophores produced by heat shocked males caused reproductive failure in females, but no significant differences among treatments were found. Our results suggest that not all traits were equally affected by the heat stress. Heat hardening did not protect reproductive traits against the negative effects of heat shock. The indirect effects of heat shock on reproduction may be equally important as the direct effects.