Does the potential strength of sexual selection differ between mating systems with and without defensive behaviours? A meta-analysis.

The Darwin-Bateman paradigm predicts that females enhance their fitness by being choosy and mating with high-quality males, while males should compete to mate with as many females as possible. In many species, males enhance their fitness by defending females and/or resources used by females. That is, males directly defend access to mating opportunities. However, paternity analyses have repeatedly shown that females in most species mate polyandrously, which contradicts traditional expectations that male defensive behaviours lead to monandry. Here, in an extensive meta-analysis, encompassing 109 species and 1026 effect sizes from across the animal kingdom, we tested if the occurrence of defensive behaviours modulates sexual selection on females and males. If so, we can illuminate the extent to which males really succeed in defending access to mating and fertilisation opportunities. We used four different indices of the opportunity for sexual selection that comprise pre-mating and/or post-mating episodes of selection. We found, for both sexes, that the occurrence of defensive behaviours does not modulate the potential strength of sexual selection. This implies that male defensive behaviours do not predict the true intensity of sexual selection. While the most extreme levels of sexual selection on males are in species with male defensive behaviours, which indicates that males do sometimes succeed in restricting females' re-mating ability (e.g. elephant seals, Mirounga leonina), estimates of the opportunity for sexual selection vary greatly across species, regardless of whether or not defensive behaviours occur. Indeed, widespread polyandry shows that females are usually not restricted by male defensive behaviours. In addition, our results indicate that post-mating episodes of selection, such as cryptic female choice and sperm competition, might be important factors modulating the opportunity for sexual selection. We discuss: (i) why male defensive behaviours fail to lower the opportunity for sexual selection among females or fail to elevate it for males; (ii) how post-mating events might influence sexual selection; and (iii) the role of females as active participants in sexual selection. We also highlight that inadequate data reporting in the literature prevented us from extracting effect sizes from many studies that had presumably collected the relevant data.

The association between personalities, alternative breeding strategies and reproductive success in dunnocks.

Although consistent between-individual differences in behaviour (i.e. animal personality) are ubiquitous in natural populations, relatively few studies have examined how personalities influence the formation of social relationships. Yet, behavioural characteristics of both sexes might be key when it comes to pair-bond formation, and cooperation with partners to successfully rear offspring. We here use a wild population of dunnocks (Prunella modularis) to first investigate whether individuals mate nonrandomly (i.e. assortative mating) with regard to four behavioural traits-flight-initiation distance (FID), provisioning, activity and vigilance-that differ in repeatability and have previously been associated with mating patterns and fitness in other species. Second, we test whether an individual's FID is associated with variability in the dunnocks' mating system (i.e. monogamous pairs vs. polygamous groups). Finally, we determine whether FID and provisioning of males and females associate with their reproductive success. We found no statistical support for assortative mating in FID between males and females. Interestingly, in polygamous groups, co-breeding males differed in their FIDs with dominant alpha males having significantly shorter FIDs compared with subordinate beta-males. Moreover, there was evidence for assortative mating in provisioning for alpha males and females in polygamous groups. We also found that male provisioning influenced reproductive success of both sexes, whereas female provisioning rates only positively correlated with her own but not their partner(s) reproductive output. Our results suggest that personality differences may have important implications for social relationships, the emergence of different mating patterns and ultimately reproductive success within populations.

Mate-guarding duration is mainly influenced by the risk of sperm competition and not by female quality in a golden orb-weaver spider.

Males are expected to mate with as many females as possible, but can maximize their reproductive success through strategic mating decisions. For instance, males can increase their own fitness by mating with high quality females that produce more offspring. Additionally, males can adjust mating effort based on the relative distribution of females and male competitors. To test factors that influence male mate choice, we assessed male mating decisions in the golden silk orb-weaver spider, Trichonephila clavipes (Nephilidae), a species in which females are polyandrous, males guard females before and after copulation occurs and large males are the most successful at guarding mates. We tested the hypothesis that males spend more time guarding high quality females that are spatially isolated, and when the risk of sperm competition is higher. We also hypothesized that this effect increases with male body size. We assessed solitary and aggregated female webs in the field and quantified female quality (i.e., female body condition), male size (i.e., male body size), the risk of sperm competition (i.e., number of males in each female web), and mate-guarding duration (i.e., number of days each male spent in each web). We found that mate-guarding behaviour is largely influenced by the presence of male competitors. In addition, male body size seems to moderately influence male guarding decisions, with larger males guarding for a longer time. Finally, female body condition and type of web (i.e., solitary or aggregated) seem to play small roles in mate-guarding behaviour. As mate-guarding duration increased by 0.718 day per each additional male competitor in the web, and guarding behaviour prevents males from seeking additional mates, it seems that guarding females can be considerably costly. We conclude that failing to guard a sexual partner promotes high costs derived from sperm competition, and a male cannot recover his relative loss in fertilization success by seeking and fertilizing more females. In addition, the search for more sexual partners can be constrained by possible high costs imposed by weight loss and fights against other males, which may explain why the type of web only moderately influenced male mate choice. Following the same rationale, if high-quality females are not easy to find and/or mating with a high-quality female demands much effort, males may search females and guard them regardless of female quality. In conclusion, the factor that most influences male mate-guarding behaviour among T. clavipes in the field is the risk of sperm competition.

Dunnock social status correlates with sperm speed, but fast sperm does not always equal high fitness.

Sperm competition theory predicts that males should modulate sperm investment according to their social status. Sperm speed, one proxy of sperm quality, also influences the outcome of sperm competition because fast sperm cells may fertilize eggs before slow sperm cells. We evaluated whether the social status of males predicted their sperm speed in a wild population of dunnocks (Prunella modularis). In addition to the traditional analysis of the average speed of sperm cells per sample, we also analysed subsamples of the fastest sperm cells per sample. In other words, we systematically evaluated the effects of including different numbers of the fastest sperm in our analyses, ranging from the 5-fastest sperm cells to the 100-fastest sperm cells in a sample. We further evaluated whether fitness, defined here as the number of chicks sired per male per breeding season, relates to the sperm speed in the same population. We found that males in monogamous pairings (i.e. low levels of sperm competition), produced the slowest sperm cells, whereas subordinate males in polyandrous male-male coalitions (i.e. high levels of sperm competition) produced the fastest sperm cells. This result was consistent regardless of the number of fastest sperm included in our analyses, but statistical support was conditional on the number of sperm cells included in the analysis. Interestingly, we found no significant relationship between fitness and sperm speed, which suggests that it is possible that the differential mating opportunities across social status levelled out any possible difference. Our study also suggests that it is important to identify biologically meaningful subsets of fastest sperm and cut-offs for inclusions for assessing sperm competition via sperm speed.

Habitat structure drives the evolution of aerial displays in birds.

John Endler's sensory drive hypothesis posits that physical properties of the environment may shape signalling traits by determining how effective they are in communicating. Evidence abounds of signalling environment driving selection on colours and vocalizations, yet little is known about its influence on visual signals produced via body movements (i.e., gestural displays). Here, we aimed to perform the most taxonomically comprehensive assessment of sensory drive by testing the hypothesis that habitat structure drives the evolution of aerial sexual displays in passerine birds (order Passeriformes). We base this hypothesis on physical properties of habitats that should allow aerial displays to transmit more broadly in open habitats. To test the hypothesis, we performed Bayesian phylogenetic comparative analyses using species-level phylogenetic trees and a dataset of 469 species from across the Americas. We found that evolutionary gain of aerial displays is on average six times more frequent in open-habitat passerines than in forest ones. The influence of habitat structure on the evolution of aerial sexual displays attests to the importance of sensory drive as a deterministic evolutionary force within sexual selection, as opposed to models that assume a purely arbitrary direction of sexual trait evolution.

Resumo A hipótese da condução sensorial de John Endler postula que propriedades físicas do ambiente podem influenciar traços de sinalização ao determinar quão efetivos eles são em comunicar. Enquanto há bastante evidência do ambiente influenciando cores e vocalizações, pouco se sabe de sua influência sobre sinais visuais produzidos por movimentos corporais (i.e., gestos). Nesse estudo, realizamos a avaliação mais taxonomicamente abrangente da condução sensorial ao testar a hipótese de que a estrutura do hábitat influencia a evolução de exibições sexuais aéreas em aves da ordem Passeriformes. Baseamos essa hipótese em propriedades físicas dos hábitats que deveriam permitir uma transmissão mais ampla de exibições aéreas em áreas abertas. Para testar a hipótese, realizamos análises comparativas filogenéticas Bayesianas utilizando árvores filogenéticas ao nível de espécie e um banco de dados de 469 espécies que ocorrem ao longo do continente americano. Encontramos que o ganho evolutivo de exibições aéreas é, em média, seis vezes mais frequente em Passeriformes de áreas abertas do que em florestais. A influência da estrutura do hábitat sobre a evolução de exibições sexuais aéreas evidencia a importância da condução sensorial como uma força evolutiva determinística dentro da seleção sexual, contrastando com modelos que predizem uma direção puramente arbitrária na evolução de traços sexuais.

Comment on "Global pattern of nest predation is disrupted by climate change in shorebirds".

Kubelka et al (Reports, 9 November 2018, p. 680) claim that climate change has disrupted patterns of nest predation in shorebirds. They report that predation rates have increased since the 1950s, especially in the Arctic. We describe methodological problems with their analyses and argue that there is no solid statistical support for their claims.

Quantitative analysis of the dose-response of white spot syndrome virus in shrimp.

White spot syndrome virus (WSSV) is an important cause of mortality and economic losses in shrimp farming. Although WSSV-induced mortality is virus dose dependent and WSSV infection does not necessarily lead to mortality, the relationships between virus-particle dose, infection and mortality have not been analysed quantitatively. Here, we explored WSSV dose-response by a combination of experiments, modelling and meta-analysis. We performed dose-response experiments in Penaeus vannamei postlarvae, recorded host mortality and detected WSSV infection. When we fitted infection models to these data, two models-differing in whether they incorporated heterogeneous host susceptibility to the virus or not-were supported for two independent experiments. To determine the generality of these results, we reanalysed published data sets and then performed a meta-analysis. We found that WSSV dose-response kinetics is indeed variable over experiments. We could not clearly identify which specific infection model has the most support by meta-analysis, but we argue that these results also are most concordant with a model incorporating varying levels of heterogeneous host susceptibility to WSSV. We have identified suitable models for analysing WSSV dose-response, which can elucidate the most basic virus-host interactions and help to avoid underestimating WSSV infection at low virus doses.

Carotenoid metabolism strengthens the link between feather coloration and individual quality.

Thirty years of research has made carotenoid coloration a textbook example of an honest signal of individual quality, but tests of this idea are surprisingly inconsistent. Here, to investigate sources of this heterogeneity, we perform meta-analyses of published studies on the relationship between carotenoid-based feather coloration and measures of individual quality. To create color displays, animals use either carotenoids unchanged from dietary components or carotenoids that they biochemically convert before deposition. We hypothesize that converted carotenoids better reflect individual quality because of the physiological links between cellular function and carotenoid metabolism. We show that feather coloration is an honest signal of some, but not all, measures of quality. Where these relationships exist, we show that converted, but not dietary, carotenoid coloration drives the relationship. Our results have broad implications for understanding the evolutionary role of carotenoid coloration and the physiological mechanisms that maintain signal honesty of animal ornamental traits.

Personality-matching habitat choice, rather than behavioural plasticity, is a likely driver of a phenotype-environment covariance.

An emerging hypothesis of animal personality posits that animals choose the habitat that best fits their personality, and that the match between habitat and personality can facilitate population differentiation, and eventually speciation. However, behavioural plasticity and the adjustment of behaviours to new environments have been a classical explanation for such matching patterns. Using a population of dunnocks (Prunella modularis), we empirically tested whether personality or behavioural plasticity is responsible for the non-random distribution of shy and bold individuals in a heterogeneous environment. We found evidence for bold individuals settling in areas with high human disturbance, but also that birds became bolder with increasing age. Importantly, personality primarily determines the distribution of individuals, and behavioural adjustment over time contributes very little to the observed patterns. We cannot, however, exclude a possibility of very early behavioural plasticity (a type of developmental plasticity) shaping what we refer to as 'personality'. Nonetheless, our findings highlight the role personality plays in shaping population structure, lending support to the theory of personality-mediated speciation. Moreover, personality-matching habitat choice has important implications for population management and conservation.

Macroecology of parental care in arthropods: higher mortality risk leads to higher benefits of offspring protection in tropical climates.

The intensity of biotic interactions varies around the world, in such a way that mortality risk imposed by natural enemies is usually higher in the tropics. A major role of offspring attendance is protection against natural enemies, so the benefits of this behaviour should be higher in tropical regions. We tested this macroecological prediction with a meta-regression of field experiments in which the mortality of guarded and unguarded broods was compared in arthropods. Mortality of unguarded broods was higher, and parental care was more beneficial, in warmer, less seasonal environments. Moreover, in these same environments, additional lines of defence further reduced offspring mortality, implying that offspring attendance alone is not enough to deter natural enemies in tropical regions. These results help to explain the high frequency of parental care among tropical species and how biotic interactions influence the occurrence of parental care over large geographic scales. Finally, our findings reveal that additional lines of defences - an oftentimes neglected component of parental care - have an important effect on the covariation between the benefits of parental care and the climate-mediated mortality risk imposed by natural enemies.

Heterogeneity in ecological and evolutionary meta-analyses: its magnitude and implications.

Meta-analysis is the gold standard for synthesis in ecology and evolution. Together with estimating overall effect magnitudes, meta-analyses estimate differences between effect sizes via heterogeneity statistics. It is widely hypothesized that heterogeneity will be present in ecological/evolutionary meta-analyses due to the system-specific nature of biological phenomena. Despite driving recommended best practices, the generality of heterogeneity in ecological data has never been systematically reviewed. We reviewed 700 studies, finding 325 that used formal meta-analysis, of which total heterogeneity was reported in fewer than 40%. We used second-order meta-analysis to collate heterogeneity statistics from 86 studies. Our analysis revealed that the median and mean heterogeneity, expressed as I2 , are 84.67% and 91.69%, respectively. These estimates are well above "high" heterogeneity (i.e., 75%), based on widely adopted benchmarks. We encourage reporting heterogeneity in the forms of I2 and the estimated variance components (e.g., τ2 ) as standard practice. These statistics provide vital insights in to the degree to which effect sizes vary, and provide the statistical support for the exploration of predictors of effect-size magnitude. Along with standard meta-regression techniques that fit moderator variables, multi-level models now allow partitioning of heterogeneity among correlated (e.g., phylogenetic) structures that exist within data.

Negative effects of prolonged dietary restriction on male mating effort: nuptial gifts as honest indicators of long-term male condition.

The handicap principle proposes that sexual signals must be costly to be honest. Honesty may be maintained by the costs paid by honest signallers or by the potential costs of cheating. In the latter, handicaps should emerge as a consequence of specific biological constraints, such as life-history trade-offs. Nuptial prey-giving arthropods are good systems to investigate the honesty of sexual signals taking into account trade-offs between self-maintenance and mating effort. We experimentally evaluated if prolonged food shortage during early adulthood imposes long-term negative effects on gift construction by males of the spider Paratrechalea ornata. We also evaluated whether a burst of food availability improved body condition of poorly fed males, increasing their frequency of gift construction. Poorly fed males hardly constructed gifts, even after a marked increase in feeding rate, which clearly improved their body condition. Moreover, initially poorly fed males that latter received high food intake constructed lighter gifts than continuously well fed males. The long-term effects of prolonged dietary restriction on male propensity to construct a gift and on the size of this gift may increase the honesty of this sexually selected signal. From the female's perspective the offer of a gift may bring information on male quality.

Conflict and cooperation over sex: the consequences of social and genetic polyandry for reproductive success in dunnocks.

Conflict and cooperation within and between the sexes are among the driving forces that lead to the evolution of mating systems. Among mating strategies, female genetic polyandry and male reproductive cooperation pose challenging evolutionary questions regarding the maintenance of systems where one sex suffers from reduced fitness. Here, we investigate the consequences of social and genetic polyandry for reproductive success of females and males in a population of the dunnock, Prunella modularis. We show that female multiple mating ameliorates the negative effects of inbreeding. We, however, found little evidence that females engage in extra-group (pair) mating with less related or more heterozygous males. Breeding in socially polyandrous groups reduced the amount of paternity lost to extra-group males, such that, on average, cobreeding and monogamous males fledged a similar number of young. Importantly, c. 30% of cobreeding male dyads were related, suggesting they could gain indirect fitness benefits. Taken together, cobreeding males achieve equivalent reproductive success to monogamous counterparts under most circumstances. Our study has revealed unexpected complexities in the variable mating system of dunnocks in New Zealand. Our results differ from the well-known Cambridge dunnock study and can help our understanding of the evolution and maintenance of various breeding systems in the animal kingdom.

Breeding biology and variable mating system of a population of introduced dunnocks (Prunella modularis) in New Zealand.

Species with variable mating systems provide a unique opportunity to investigate whether females receive direct fitness benefits from additional male partners. The direct benefits provide an obvious explanation for why females would breed polyandrously, in a situation where males clearly do not attain their optimal reproductive success. Evidence for these direct benefits is, however, mixed. Here, we present a detailed study of the breeding biology of the dunnock, Prunella modularis, which inform an investigation into the effects of the social mating system on the reproductive success in a population of dunnocks in Southern New Zealand. We studied 80 different social groups over the course of three breeding seasons. Dunnocks in our population presented a variable mating system, with socially monogamous (45%), socially polyandrous (54%) and socially polygynandrous (1%) groups being observed in the same breeding season. We did not observe any polygynous social units in our study period although polygyny exists in the population. We found little difference in the numbers of eggs laid, and egg volume between monogamous and polyandrous nests. However, polyandrous groups had better hatching and fledging success than monogamous groups (composite d = 0.385, 95% CI: 0.307 to 0.463). Overall our results support the notion that polyandry is beneficial for females.