Predators live a remarkable life encountering, chasing, and hunting prey. Beyond eating their prey, however, predators also alter prey fitness by scaring them. Recent research estimates fear of predators inflicts equal or more adverse effects on prey demography compared to being consumed by predators. They do so altering fitness-influencing behaviours such as foraging and reproduction. Although fear effects are known to influence fitness by affecting individual reproductive decisions, how these changes scale-up to affect the prey mating patterns at the population level remains largely unknown. We developed and empirically tested a new conceptual framework that predicts how predation risk may affect mating patterns, specifically size assortative mating (SAM), in prey populations.

We developed two mutually inclusive hypothesis based on perception of fear by prey. Typically, predation risk is thought to increase the immediate costs of engaging in reproductive behaviors such as sexual signalling, fighting, and searching for mates. This is because individuals engaged in these conspicuous breeding activities may stand out, and may not survive when attacked. To reduce this immediate risk, prey may engage less in reproductive behaviors aimed at assessing mate quality and become less choosy. This could lead to less discriminant mating, thereby disrupting prey SAM.

Predation risk may affect mating patterns also by reducing the expected reproductive benefits of choosing to pair with a certain mate. Both parents and offspring that reside in risky patches may experience lower survival and suffer long-term fear effects. Consequently, prey individuals in risky patches are expected to have lower lifetime fitness than those from safer habitats. Therefore, prey is expected to show lesser preference for mates of equal innate quality that inhabit risky locations. Since body size is positively associated with fitness in many species, we hypothesized that the largest individuals inhabiting safe sites should have the highest reproductive value, and the smallest individuals inhabiting risky sites should have the lowest value. Between those two extremes, we expected smaller individuals in safer habitats and larger individuals in riskier sites to have similar reproductive values. Considering only this long-term predation effect, we predicted no change in the strength of SAM, but expected that in risky sites the choosing sex will be on average smaller for a given mate size.

To test these ideas we performed manipulative field experiment testing how risk of Israeli gold scorpion predation affects mating patterns of the desert isopod. Desert isopods are fascinating as they mate only once in their life and spend the rest of their life with the chosen mate and their family in a single permanent burrow. Isopod females initiate the burrows, and the males actively choose and fight over them, yielding an evident SAM. Both parents exhibit elaborate parental care. Thus, burrow location and mate quality are critical fitness determinants in this species.

We drilled holes into the soil to attract wild isopod females to found burrows. We established active scorpion burrows near half of the isopod burrows and monitored isopod pair formation till all isopods had settled. Before the end of the development period of their offspring, we collected all isopods and measured the parents’ sizes, and the embryos’ size, age, and number. This allowed us to measure fitness consequences of choosing certain mates in certain habitats. Also, to better understand how these patterns emerge, we conducted a complementary experiment testing how predation risk affects reproductive behaviors of male isopods. We introduced two males of different sizes to a field arena that included two females of similar sizes inhabiting burrows that were near or away from predator cues, and monitored isopod behavior.

We found that fewer isopod pairs were established in burrows in risky environments. Predation risk did not disrupt the SAM, but males in risky environments were on average smaller for a given female size. Therefore, risk of predation showed no evident reduction in discriminant mating. Instead, these findings supported our novel hypothesis that males anticipated future costs of predation and used this information to lessen the expected reproductive benefits that are based solely on mate size. Furthermore, isopod females (i.e., burrow initiators) were of similar sizes near and away from scorpion burrows suggesting that they do not compete for burrows. There was no effect of predation risk on the average number, size, or age of progeny. Number of eggs were positively correlated with female size, corroborating what is well-known in many species, and attributing reason to why males may be competing for access to large females. To gain a better mechanistic understanding, we explored how males of different sizes respond to similar size females that occupied burrows near and away from predator cues. We found that larger males stayed for longer duration near safe burrows and won more male-male encounters than smaller conspecifics.

Our results provide first empirical evidence that predation risk may regulate population level mating patterns by reducing the expected long-term reproductive values of potential mates and the mechanism underlying this pattern is male-male competition.