A systematic map of studies testing the relationship between temperature and animal reproduction

1. Exposure to extreme temperatures can negatively affect animal reproduction, by disrupting the ability of individuals to produce any offspring (fertility), or the number of offspring produced by fertile individuals (fecundity). This has important ecological consequences, because reproduction is the ultimate measure of population fitness: a reduction in reproductive output lowers the population growth rate and increases the extinction risk. Despite this importance, there have been no large-scale summaries of the evidence for effect of temperature on reproduction. 2. We provide a systematic map of studies testing the relationship between temperature and animal reproduction. We systematically searched for published studies that statistically test for a direct link between temperature and animal reproduction, in terms of fertility, fecundity or indirect measures of reproductive potential (gamete and gonad traits). 3. Overall, we collated a large and rich evidence base, with 1654 papers that met our inclusion criteria, encompassing 1191 species. 4. The map revealed several important research gaps. Insects made up almost half of the dataset, but reptiles and amphibians were uncommon, as were non-arthropod invertebrates. Fecundity was the most common reproductive trait examined, and relatively few studies measured fertility. It was uncommon for experimental studies to test exposure of different life stages, exposure to short-term heat or cold shock, exposure to temperature fluctuations, or to independently assess male and female effects. Studies were most often published in journals focusing on entomology and pest control, ecology and evolution, aquaculture and fisheries science, and marine biology. Finally, while individuals were sampled from every continent, there was a strong sampling bias towards mid-latitudes in the Northern Hemisphere, such that the tropics and polar regions are less well sampled. 5. This map reveals a rich literature of studies testing the relationship between temperature and animal reproduction, but also uncovers substantial missing treatment of taxa, traits, and thermal regimes. This database will provide a valuable resource for future quantitative meta-analyses, and direct future studies aiming to fill identified gaps

Rapid shift in thermal resistance between generations through maternal heat exposure

Given the current rapid climate change, understanding the mechanisms underlying heat tolerance and its plasticity is an important goal of global change biology. Soil fauna communities are especially vulnerable because of their limited dispersal ability. It is generally recognized that transgenerational effects can contribute to the expression of phenotypic plasticity. Nevertheless, transgenerational plasticity in belowground organisms has received relatively little attention in the context of climate change, despite their major role in soil functioning. Here we test for transgenerational effects of heat shock exposure in the soil arthropod Orchesella cincta, a springtail species that regularly experiences heat stress conditions in its natural environment. We exposed females to heat stress, and subsequently investigated the effects of the same stress on the survival of their offspring. Thermal resistance of the progeny from treated and untreated mothers was compared at three life stages: egg, juvenile and adult. We provide evidence that exposure to heat shock induces a life stage-dependent increase in thermal resistance in the subsequent generation. The induced adaptive maternal effect persisted into the adult stage of the progeny. However, there is also a tradeoff resulting in reduced clutch size of treated females. These results are of broad significance to understanding the potential of organisms to cope with a changing climate

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 1 h), heat shock (37.2. °C for 1 h), heat hardening. +. heat shock (35.2. °C for 1 h, followed 15 h later by 37.2. °C for 1 h), 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. © 2011 Elsevier Ltd

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

Different sperm number in the spermatophores of Orchesella villosa (Geoffroy) (Entomobryidae) and Allacma fusca (L.) (Sminthuridae)

Members of the basal hexapod group Collembola perform indirect sperm transfer; males deposit spermatophores on the soil and these are then picked up by females for insemination. Orchesella villosa exhibits a dissociated mating behavior, while Allacma fusca has either associated mating behavior or, more commonly, produces spermatophores without pairing. Sperm ultrastructure in the two species has been studied by TEM and SEM observations to estimate the volume of these cells. The sperm number into each spermatophore has been determined by counting the .fluorescent nuclei after Hoechst staining of sperm droplets squash preparations. Sperm droplets at the apex of spermatophores contain numerous spermatozoa of typical appearance, wound up and with a long anterior appendage (peduncle). Sperm droplets of Orchesella villosa are smaller (about 10 times) than in A. fusca, however they contain substantially more sperm cells (about three times). These differences could be explained as follows: (a) sperm of O. villosa are shorter than those of A. fusca (58 and 107 mm, respectively) and thus the volume of a single sperm of O. villosa is about 10 times smaller than in A. fusca; (b) considering the volume of sperm droplets and of sperm cells, the estimated number of sperm cells would be higher in A. fusca than in O. villosa; and (c) the conspicuous reduction of the sperm cells observed in A. fusca is likely linked to the aberrant meiosis present in this species, as well as in all Symphypleona studied so far, that causes a loss of 50% of their sperm

The ultrastructure of the spermathecae in the Collembola Symphypleona (Hexapoda)

The fine structure of the paired spermathecae of two Symphypleona Collembola, Sminthurus viridis and Allacma fusca, was studied. The spermathecal epithelium is rich in pigment granules, while secretory organelles are scarce, consisting of a few mitochondria and microtubules, scattered cisterns of endoplasmic reticulum and Golgi systems. Small isolated secretory granules are visible in the apical cell region, where irregular microvilli are present. Beneath the epithelium, large cells rich in endoplasmic reticulum and Golgi systems are present; they are separated from the epithelial cells by a thin basal lamina. The epithelium is lined by a thin cuticle, which forms thin extensions at the beginning of the spermathecal duct. At this level, muscle fibers are visible. The spermathecal lumen is filled with many spermatozoa. At molting, the spermathecal epithelial cells detach from the cuticle and a large electrontransparent space is evident between the cytoplasm and the cuticle. The cytoplasm has few pigment granules and the spermathecal lumen contains degenerating spermatozoa. After 3 days, the spermathecal epithelium regains its usual appearance and the spermathecal lumen is empty. The two species of Collembola Symphypleona do not have accessory glands. Compared with the Arthropleona Orchesella villosa, which has a single spermatheca and two accessory glands (Dallai et al. [2008] J Morphol 269:464–478), a great difference has occurred in the organization of the female genital system of these species. The results are discussed in light of the implications for reproductive behavior and egg protection in Symphypleona

Transgenerational effects of nutrition are different for sons and daughters

Food shortage is an important selective factor shaping animal life-history trajectories. Yet, despite its role, many aspects of the interaction between parental and offspring food environments remain unclear. In this study, we measured developmental plasticity in response to food availability over two generations and tested the relative contribution of paternal and maternal food availability to the performance of offspring reared under matched and mismatched food environments. We applied a cross-generational split-brood design using the springtail Orchesella cincta, which is found in the litter layer of temperate forests. The results show adverse effects of food limitation on several life-history traits and reproductive performance of both parental sexes. Food conditions of both parents contributed to the offspring phenotypic variation, providing evidence for transgenerational effects of diet. Parental diet influenced sons’ age at maturity and daughters’ weight at maturity. Specifically, being born to food-restricted parents allowed offspring to alleviate the adverse effects of food limitation, without reducing their performance under well-fed conditions. Thus, parents raised on a poor diet primed their offspring for a more efficient resource use. However, a mismatch between maternal and offspring food environments generated sex-specific adverse effects: female offspring born to well-fed mothers showed a decreased flexibility to deal with low-food conditions. Notably, these maternal effects of food availability were not observed in the sons. Finally, we found that the relationship between age and size at maturity differed between males and females and showed that offspring life-history strategies in O. cincta are primed differently by the parents

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 productioninfluence female choice. We found that Orchesella males display plasticity in spermatophore allocation. Males decreased the spermatophorenumber 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. © 2013 The Author(s) Published by the Royal Society. All rights reserved