Animals are usually expected to avoid mating with relatives (kin avoidance) as incestuous mating can lead to the expression of inbreeding depression. Yet, theoretical models predict that unbiased mating with regards to kinship should be common, and that under some conditions, the inclusive fitness benefits associated with inbreeding can even lead to a preference for mating with kin. This mismatch between empirical and theoretical expectations generates uncertainty as to the prevalence of inbreeding avoidance in animals. Here, we synthesized 677 effect sizes from 139 experimental studies of mate choice for kin versus non-kin in diploid animals, representing 40 years of research, using a meta-analytical approach. Our meta-analysis revealed little support for the widely held view that animals avoid mating with kin, despite clear evidence of publication bias. Instead, unbiased mating with regards to kinship appears widespread across animals and experimental conditions. The significance of a variety of moderators was explored using meta-regressions, revealing that the degree of relatedness and prior experience with kin explained some variation in the effect sizes. Yet, we found no difference in kin avoidance between males and females, choice and no-choice experiments, mated and virgin animals or between humans and animals. Our findings highlight the need to rethink the widely held view that inbreeding avoidance is a given in experimental studies.

Meta-analytic evidence that animals rarely avoid inbreeding

Despite increasing evidence of the importance of repeatable among-individual differences in behaviour (animal personality) in ecology and evolution, little remains known about the role of animal personalities in sexual selection. Here, we present an investigation of the hypothesis that the personalities of individuals and their sexual partners play a role in different episodes of sexual selection, and the extent to which these effects are modulated by the social environment. We first examined how two repeatable behaviours-exploration and boldness-are associated with pre- and postcopulatory sexual selection in male red junglefowl Gallus gallus, using replicate groups across three experimental sex ratio treatments. We further explored how the social environment modulates relationships between male personality and mating performance, and whether mating is assortative or disassortative with respect to exploration or boldness. Finally, we examined behavioural mechanisms linking personality with mating performance. Across all sex ratios, the fastest and slowest exploring males courted females proportionally less, and faster exploring males associated with females more and received more sexual solicitations. In female-biased groups, the fastest and slowest exploring males experienced the highest mating success and lowest sperm competition intensity. Faster exploring males also obtained more mates in female-biased groups when their competitors were, on average, slower exploring, and the proportion of matings obtained by fast-exploring males decreased with the proportion of fast-exploring males in a group, consistent with negative frequency-dependent sexual selection. While boldness did not predict mating performance, there was a tendency for individuals to mate disassortatively with respect to boldness. Collectively, our results suggest that male exploration can play a role in sexual selection, and that sexual selection on personality is complex and contingent on the social environment.

https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/1365-2656.13454

Sexual selection and personality: Individual and group-level effects on mating behaviour in red junglefowl.

Intra-individual stable but inter-individually variable behaviours, i.e. personalities, are commonly reported across diverse animal groups, yet the reasons for their maintenance remain controversial. Therefore, studying fitness consequences of personality traits is necessary to discriminate between alternative explanations. Here, I measured boldness, a highly repeatable personality trait, and reproductive success in male guppies, Poecilia reticulata. I found that bolder males had higher reproductive success than their shyer conspecifics and they sired offspring with females who had larger clutches. This result provides direct evidence for fitness consequences of boldness in the guppy. It suggests that the effect may be driven by bolder males mating with more fecund females.

/pdf/bolder-guppies-do-not-have-more-mating-partners-yet-sire-355lwb7zgo.pdf

Bolder guppies do not have more mating partners, yet sire more offspring

Measures of cognitive performance, derived from psychometric tasks, have yielded important insights into the factors governing cognitive variation. However, concerns remain over the robustness of these measures, which may be susceptible to non-cognitive factors such as motivation and persistence. Efforts to quantify short-term repeatability of cognitive performance have gone some way to address this, but crucially the long-term repeatability of cognitive performance has been largely overlooked. Quantifying the long-term repeatability of cognitive performance provides the opportunity to determine the stability of cognitive phenotypes and the potential for selection to act on them. To this end, we quantified long-term repeatability of cognitive performance in wild Australian magpies over a three-year period. Cognitive performance was repeatable in two out of four cognitive tasks—associative learning and reversal-learning performance was repeatable, but spatial memory and inhibitory control performance, although trending toward significance, was not. Measures of general cognitive performance, obtained from principal components analyses carried out on each cognitive test battery, were highly repeatable. Together, these findings provide evidence that at least some cognitive phenotypes are stable, which in turn has important implications for our understanding of cognitive evolution.

Long-term repeatability of cognitive performance

Temperature-driven changes in behavioural unpredictability and personality in the beadlet sea anemone, Actinia equina

Assessing the consequences of personality traits on reproductive success is one of the most important challenges in personality studies and critical to understand the evolutionary implications of behavioural variability among animals. Personality traits are typically associated with mating acquisition in males, and, hence, linked to variation in their reproductive success. However, in most species, sexual selection continues after mating, and sperm traits (such as sperm number and quality) become very important in determining post-mating competitive success. Here, we investigate whether variation in personality traits is associated with variation in sperm traits using the guppy (Poecilia reticulata), a species with high levels of sperm competition. We found a positive association between boldness and sperm number but not sperm velocity, suggesting that bolder males have increased post-copulatory success than shyer individuals. No association was found between exploration and sperm traits. Our work highlights the importance of considering post-copulatory traits when investigating fitness consequences of personality traits, especially in species with high levels of female multiple matings and hence sperm competition.

https://royalsocietypublishing.org/doi/pdf/10.1098/rsos.190474

The bold and the sperm: positive association between boldness and sperm number in the guppy.

Female Western Australian magpies discriminate between familiar and unfamiliar human voices

Female guppies increase their propensity for polyandry as an inbreeding avoidance strategy

Repeated testing does not confound cognitive performance in the Western Australian magpie (Cracticus tibicen dorsalis)

Recent research has highlighted how trappability and self-selection—the processes by which individuals with particular traits may be more likely to be caught or to participate in experiments—may be sources of bias in studies of animal behaviour and cognition. It is crucial to determine whether such biases exist, and if they do, what effect they have on results. In this study, we investigated if trappability (quantified through ‘ringing status’—whether or not a bird had been trapped for ringing) and self-selection are sources of bias in a series of associative learning experiments spanning 5 years in the Western Australian magpie (Gymnorhina tibicen dorsalis). We found no evidence of self-selection, with no biases in task participation associated with sex, age, group size or ringing status. In addition, we found that there was no effect of trappability on cognitive performance. These findings give us confidence in the results generated in the animal cognition literature and add to a growing body of literature seeking to determine potential sources of bias in studies of animal behaviour, and how they influence the generalizability and reproducibility of findings.

Elizabeth M. Speechley

Papers

The bold and the sperm: positive association between boldness and sperm number in the guppy.

Female Western Australian magpies discriminate between familiar and unfamiliar human voices

Female guppies increase their propensity for polyandry as an inbreeding avoidance strategy

Repeated testing does not confound cognitive performance in the Western Australian magpie (Cracticus tibicen dorsalis)

Does trappability and self-selection influence cognitive performance?