Sexual selection favours male parental care, when females can choose

Explaining the evolution of male care has proved difficult. Recent theory predicts that female promiscuity and sexual selection on males inherently disfavour male care. In sharp contrast to these expectations, male-only care is often found in species with high extra-pair paternity and striking variation in mating success, where current theory predicts female-only care. Using a model that examines the coevolution of male care, female care and female choice; I show that inter-sexual selection can drive the evolution of male care when females are able to bias mating or paternity towards parental males. Surprisingly, female choice for parental males allows male care to evolve despite low relatedness between the male and the offspring in his care. These results imply that predicting how sexual selection affects parental care evolution will require further understanding of why females, in many species, either do not prefer or cannot favour males that provide care.     

Sexual selection when fertilization is not guaranteed

Abstract Much of the theory of sexual selection assumes that females do not generally experience difficulties getting their eggs fertilized, yet sperm limitation is occasionally documented. How often does male limitation form a selection for female traits that improve their mating rate? The question is difficult to test, because if such traits evolve to be efficient, sperm limitation will no longer appear to be a problem to females. Here, we suggest that changes in choosiness between populations, and in particular between virgin and mated females, offer an efficient way to test this hypothesis. We model the “wallflower effect,” that is, changes in female preferences due to time and mortality costs of remaining unmated (for at least some time). We show that these costs cause adaptive reductions of female choice, even if mate encounter rates appear high and females only rarely end their lives unfertilized. We also consider the population consequences of plastic or fixed mate preferences at different mate encounter rates. If mate choice is plastic, we confirm earlier verbal models that virgins should mate relatively indiscriminately, but plastic increase of choosiness in later matings can compensate and intensify sexual selection on the male trait, particularly if there is last male sperm precedence. Plastic populations will cope well with unusual conditions: eagerness of virgins leads to high reproductive output and a relaxation of sexual selection at low population densities. If females lack such plasticity, however, population‐wide reproductive output may be severely reduced, whereas sexual selection on male traits remains strong.     

Sexual selection in the monogamous barn swallow (Hirundo rustica). II. Mechanisms of sexual selection

Mechanisms of sexual selection in the monogamous, sexually dimorphic barn swallow (Hirundo rustica) were studied during a seven-year period. First, the sex ratio of reproducing adults was male-biased, and mated males had significantly longer tail ornaments than unmated males. Secondly, some of the unmated individuals later committed infanticide and became mated with the mother of the killed brood. Fathers of killed broods had significantly shorter tails than other males, and there was a tendency for infanticidal males to have longer tail ornaments than other unmated males. Thirdly, long-tailed male barn swallows were more successful in acquiring extra-pair copulations than other males, and females involved in extra-pair copulations, as compared to females not involved in such copulations, had mates with shorter tail ornaments. Fourthly, male barn swallows having long tails as compared to short-tailed males acquired mates in better body condition. Females mated to long-tailed males reproduced earlier, laid more eggs and were more likely to have two clutches than were females mated to short-tailed males. Finally, females mated to long-tailed males put more effort into reproduction than did other females, as evidenced by their relatively larger contribution to feeding of offspring. Thus, at least five different components of sexual selection affected male reproductive success. Selection arising from differential success during extra-pair copulations, differential reproductive success and differential male reproductive effort thus accounted for most of the selection on tail ornaments in male barn swallows.     

Sexual cannibalism by Octopus cyanea on a Pacific coral reef

Sexual cannibalism is rare in the animal kingdom. Although cannibalism is not uncommon in cephalopods, here we report the first documented case of sexual cannibalism. A large female Octopus cyanea was observed continuously for 2.5 days in Palau, Micronesia, when she was out of her den. On the second day, a small male followed and mated her 13 times during 3.5 h while she continued to forage over 70 m distance. After the 12th mating, she aggressively chased a different small octopus that barely escaped by jetting, inking and swimming upwards. Shortly thereafter, the original small male mated her a 13th time, but subsequently she attacked and suffocated him and spent 2 days cannibalizing him in her den. This sort of intraspecific aggression helps to explain several reports of octopuses mating out in the open, a behaviour that may serve to allow the smaller mate to escape cannibalism.     

Sexual cannibalism by Octopus cyanea on a Pacific coral reef

Sexual cannibalism is rare in the animal kingdom. Although cannibalism is not uncommon in cephalopods, here we report the first documented case of sexual cannibalism. A large female Octopus cyanea was observed continuously for 2.5 days in Palau, Micronesia, when she was out of her den. On the second day, a small male followed and mated her 13 times during 3.5 h while she continued to forage over 70 m distance. After the 12th mating, she aggressively chased a different small octopus that barely escaped by jetting, inking and swimming upwards. Shortly thereafter, the original small male mated her a 13th time, but subsequently she attacked and suffocated him and spent 2 days cannibalizing him in her den. This sort of intraspecific aggression helps to explain several reports of octopuses mating out in the open, a behaviour that may serve to allow the smaller mate to escape cannibalism.     

Different mate preferences by parasitized and unparasitized females potentially reduces sexual selection

Parasite‐mediated models of sexual selection predict that females should avoid parasitized mates, thereby generating selection on male traits revealing health. The strength of this selection, however, may depend on the prevalence of parasitism among females if their infection status alters their mate preferences. We evaluated the effects of a socially transmitted parasite on male traits and female behaviour in spadefoot toads. Parasitized males were larger and in better condition than unparasitized males. Moreover, better condition males produced longer calls. Unparasitized females preferred longer calls indicative of good‐condition males that are more likely parasitized. By contrast, parasitized females as a group possessed no preference for call duration. Presumably because of reduced selection by these parasitized females, male mating success was not associated with any measured traits. Thus, when females are parasitized, sexual selection on condition‐dependent traits is potentially reduced.     

Stronger convex (stabilizing) selection on homologous sexual display traits in females than in males: a multipopulation comparison in Drosophila serrata

Mutual mate choice for homologous sexual display traits has been demonstrated in several recent studies yet little attention has been given to quantitative comparison of the strength and form of mate preferences between the sexes. Such comparisons may provide important insight into the evolution of mate choice for honest signals. In particular, because females generally provide the majority of resources for initial offspring development, female displays may trade-off with fecundity, causing preference evolution to differ between the sexes. Recent theory suggests that adaptive male preferences for honest displays in females are possible under certain conditions and may result in preferences that are convex (i.e., stabilizing) in form. We compared sexual selection on a suite of contact pheromones arising from mutual mate choice using nine separate geographic populations of Drosophila serrata. We show that the convex selection is stronger on females than on males overall in these populations, and that convex selection is the predominate form of nonlinear selection on females but not males.     

Sexual selection in a lekking bird: the relative opportunity for selection by female choice and male competition

Leks are classic models for studies of sexual selection due to extreme variance in male reproductive success, but the relative influence of intrasexual competition and female mate choice in creating this skew is debatable. In the lekking lance-tailed manakin (Chiroxiphia lanceolata), these selective episodes are temporally separated into intrasexual competition for alpha status and female mate choice among alpha males that rarely interact. Variance in reproductive success between status classes of adult males (alpha versus non-alpha) can therefore be attributed to male-male competition whereas that within status largely reflects female mate choice. This provides an excellent opportunity for quantifying the relative contribution of each of these mechanisms of sexual selection to the overall opportunity for sexual selection on males (I males). To calculate variance in actual reproductive success, we assigned genetic paternity to 92.3% of 447 chicks sampled in seven years. Reproduction by non-alphas was rare and apparently reflected status misclassifications or opportunistic copulations en route to attaining alpha status rather than alternative mating strategies. On average 31% (range 7-44%, n=6 years) of the total I males was due to variance in reproductive success between alphas and non-alphas. Similarly, in a cohort of same-aged males followed for six years, 44-58% of the total I males was attributed to variance between males of different status. Thus, both intrasexual competition for status and female mate choice among lekking alpha males contribute substantially to the potential for sexual selection in this species.     

Sexual selection and animal personality

Consistent individual behavioural tendencies, termed “personalities”, have been identified in a wide range of animals. Functional explanations for personality have been proposed, but as yet, very little consideration has been given to a possible role for sexual selection in maintaining differences in personality and its stability within individuals. We provide an overview of the available literature on the role of personality traits in intrasexual competition and mate choice in both human and non‐human animals and integrate this into a framework for considering how sexual selection can generate and maintain personality. For this, we consider the evolution and maintenance of both main aspects of animal personality: inter‐individual variation and intra‐individual consistency.     

Sexual selection and genetic colour polymorphisms in animals

Genetic colour polymorphisms are widespread across animals and often subjected to complex selection regimes. Traditionally, colour morphs were used as simple visual markers to measure allele frequency changes in nature, selection, population divergence and speciation. With advances in sequencing technology and analysis methods, several model systems are emerging where the molecular targets of selection are being described. Here, we discuss recent studies on the genetics of sexually selected colour polymorphisms, aiming at (i) reviewing the evidence of sexual selection on colour polymorphisms, (ii) highlighting the genetic architecture, molecular and developmental basis underlying phenotypic colour diversification and (iii) discuss how the maintenance of such polymorphisms might be facilitated or constrained by these. Studies of the genetic architecture of colour polymorphism point towards the importance of tight clustering of colour loci with other trait loci, such as in the case of inversions and supergene structures. Other interesting findings include linkage between colour loci and mate preferences or sex determination, and the role of introgression and regulatory variation in fuelling polymorphisms. We highlight that more studies are needed that explicitly integrate fitness consequences of sexual selection on colour with the underlying molecular targets of colour to gain insights into the evolutionary consequences of sexual selection on polymorphism maintenance.     

Changed environmental conditions weaken sexual selection in sticklebacks

Environmental heterogeneity can cause the intensity and direction of selection to vary in time and space. Yet, the effects of human-induced environmental changes on sexual selection and the expression of mating traits of native species are poorly known. Currently, the breeding habitats of the three-spined stickleback Gasterosteus aculeatus are changing in the Baltic Sea because of eutrophication and increased growth of algae. Here we show that enhanced growth of filamentous algae increases the costs of mating by inducing an increase in the time and energy spent on courtship and mate choice. This is not followed by a concomitant increase in mate attraction, but instead the strength of selection on male red nuptial coloration and courtship activity is relaxed. Thus, the high investment into the costly sexually selected traits is maladaptive under the new conditions, and the mating system mediates a negative effect of the environmental change on the population. We attribute these environmentally induced changes in the benefit of the mating traits and in the strength of sexual selection to reduced visibility in dense vegetation. Anthropogenic disturbances hence affect the selection pressures that mould the species, which could have long-term effects on the viability and evolution of the populations.     

Spatial environmental complexity mediates sexual conflict and sexual selection in Drosophila melanogaster

Sexual selection is an important agent of evolutionary change, but the strength and direction of selection often vary over space and time. One potential source of heterogeneity may lie in the opportunity for male–male and/or male–female interactions imposed by the spatial environment. It has been suggested that increased spatial complexity permits sexual selection to act in a complementary fashion with natural selection (hastening the loss of deleterious alleles and/or promoting the spread of beneficial alleles) via two (not mutually exclusive) pathways. In the first scenario, sexual selection potentially acts more strongly on males in complex environments, allowing males of greater genetic “quality” a greater chance of outcompeting rivals, with benefits manifested indirectly in offspring. In the second scenario, increased spatial complexity reduces opportunities for males to antagonistically harm females, allowing females (especially those of greater potential fecundities) to achieve greater reproductive success (direct fitness benefits). Here, using Drosophila melanogaster, we explore the importance of these mechanisms by measuring direct and indirect fitness of females housed in simple vial environments or in vials in which spatial complexity has been increased. We find strong evidence in favor of the female conflict‐mediated pathway as individuals in complex environments remated less frequently and produced more offspring than those housed in a simpler spatial environment, but no difference in the fitness of sons or daughters. We discuss these results in the context of other recent studies and what they mean for our understanding of how sexual selection operates.     

Hungry females show stronger mating preferences

Female mating decisions that are based on condition-dependenttraits, such as male nutritional state, may be associated witha female's own condition. In the swordtail fish, Xiphophorusbirchmanni, females prefer the chemical cues of well-fed malesto cues of food-deprived males. Here we show that this preferenceis significantly stronger in females when they were experimentallyfood deprived than when they were well fed. Our results suggestthat if females have limited access to food resources, and arethemselves food deprived, they will attend to cues indicatingmale nutritional condition more than when environmental conditionsallow for greater access to food. Furthermore, not only is theslope of the preference function condition dependent but also,in all trials, the latency to respond to the presented stimuliwas shorter in food-deprived females, suggesting that responsivenessto environmental cues is condition dependent as well. Undernatural conditions, females of many species likely experiencevariation in resource availability. Thus, we predict that covariancebetween the strength of female preferences and resource availabilitymay be widespread and may represent a common source of femalepreference variation within and between populations.     

Sexual selection research on spiders: progress and biases

The renaissance of interest in sexual selection during the last decades has fuelled an extraordinary increase of scientific papers on the subject in spiders. Research has focused both on the process of sexual selection itself, for example on the signals and various modalities involved, and on the patterns, that is the outcome of mate choice and competition depending on certain parameters. Sexual selection has most clearly been demonstrated in cases involving visual and acoustical signals but most spiders are myopic and mute, relying rather on vibrations, chemical and tactile stimuli. This review argues that research has been biased towards modalities that are relatively easily accessible to the human observer. Circumstantial and comparative evidence indicates that sexual selection working via substrate-borne vibrations and tactile as well as chemical stimuli may be common and widespread in spiders. Pattern-oriented research has focused on several phenomena for which spiders offer excellent model objects, like sexual size dimorphism, nuptial feeding, sexual cannibalism, and sperm competition. The accumulating evidence argues for a highly complex set of explanations for seemingly uniform patterns like size dimorphism and sexual cannibalism. Sexual selection appears involved as well as natural selection and mechanisms that are adaptive in other contexts only. Sperm competition has resulted in a plethora of morphological and behavioural adaptations, and simplistic models like those linking reproductive morphology with behaviour and sperm priority patterns in a straightforward way are being replaced by complex models involving an array of parameters. Male mating costs are increasingly being documented in spiders, and sexual selection by male mate choice is discussed as a potential result. Research on sexual selection in spiders has come a long way since Darwin, whose spider examples are reanalysed in the context of contemporary knowledge, but the same biases and methodological constraints have persisted almost unchanged through the current boom of research.     

Sexual selection on Drosophila serrata male pheromones does not vary with female age or mating status

Mate preferences are costly and are thought to evolve due to the direct and/or indirect benefits they provide. Such costs and benefits may vary in response to intrinsic and extrinsic factors with important evolutionary consequences. Limited attention has been given to quantifying such variation and understanding its causes, most notably with respect to the direction and strength of preferences for multivariate sexual displays. In Drosophila serrata, female preferences target a pheromone blend of long‐chain cuticular hydrocarbons (CHCs). We used a factorial design to test whether female age and mating status generated variation in the strength and direction of sexual selection on male CHCs. Replicate choice mating trials were conducted using young and old females (4 or 10 days post‐emergence) that were either virgin or previously mated. The outcome of such trials is known to capture variation in female mate preferences, although male–male interactions may also contribute. Directional sexual selection on male CHCs was highly significant within each treatment, but there was little evidence of any variation among treatments. The absence of treatment effects implies that the multivariate combination of male CHCs preferred by females was constant with respect to female age and mating status. To the extent that male–male interactions may also contribute, our results similarly imply that these did not vary among treatments groups. With respect to D. serrata mate preferences, our results suggest that either plasticity with respect to age and mating status is not beneficial to females, or preference expression is somehow constrained.     

Juvenile infection and male display: testing the bright male hypothesis across individual life histories

Current tests of the bright male hypothesis focus on assaysof adult disease resistance and their relation to male traitdevelopment and female choice. We suggest that if parasiteshave significant harmful effects on juvenile stages of a host,then females selecting males that effectively signal juvenileparasite resistance may gain a significant "good genes" benefit.Currently, there is no information on juvenile and adult infectionor resistance in the same male and whether adult male displayssignal juvenile parasite resistance. In the present study, wemeasure infection of the ectoparasitic louse, Myrsidea ptilonorhynchi,in individual male satin bowerbirds (Ptilonorhynchus violaceus)both as juveniles and nine or more years later as adults. Wetest hypotheses that examine the role of juvenile parasite infectionin mediating sexual selection. We found that (1) juvenile infectionis higher than adult infection in the same individuals, (2)adult males able to hold display sites have lower juvenile infection,and (3) juvenile and adult infection in the same individualsare not significantly correlated. In addition, comparisons amonga larger set of individuals from a single year show that bloodand ectoparasite infections are highly correlated, and bothdecrease with male age and are inversely related to male courtshipsuccess. These results, combined with the evidence that femalesmate exclusively with bower-holding males support the hypothesisthat females use adult male display traits to identify maleswith a high level of juvenile disease resistance. We suggestthat effective tests of the bright male hypothesis should include(1) assessment of infection resistance in both subadult andadult life history stages, (2) tests of whether differencesin age-specific resistance are indicated in adult male displays,and (3) tests to determine if females attend to these traitsin mate choice. Although these requirements increase the difficultyof testing the bright male hypothesis, they are necessary fora more accurate assessment of the effects of parasites on maledisplay and female choice.     

Male choice generates stabilizing sexual selection on a female fecundity correlate

We know very little about male mating preferences and how they influence the evolution of female traits. Theory predicts that males may benefit from choosing females on the basis of traits that indicate their fecundity. Here, we explore sexual selection generated by male choice on two components of female body size (wing length and body mass) in Drosophila serrata. Using a dietary manipulation to alter female size and 828 male mate choice trials, we analysed linear and nonlinear sexual selection gradients on female mass and wing length. In contrast to theoretical expectations and prevailing empirical data, males exerted stabilizing rather than directional sexual selection on female body mass, a correlate of fecundity. Sexual selection was detected only among females with access to standard resource levels as an adult, with no evidence for sexual selection among resource-depleted females. Thus the mating success of females with the same body mass differed depending upon their access to resources as an adult. This suggests that males in this species may rely on signal traits to assess body mass rather than assessing it directly. Stabilizing rather than directional sexual selection on body mass together with recent evidence for stabilizing sexual selection on candidate signal traits in this species suggests that females may trade-off resources allocated to reproduction and sexual signalling.