Sexual selection and cuckoldry in a monogamous songbird: implications for sexual selection theory

Sexual selection is generally assumed to be weaker in monogamous than in polygynous animals. Recently, though, extra-pair fertilizations have been hailed as an important force in generating variance in reproductive success among males in socially monogamous species, thereby increasing the intensity of sexual selection. To see if extra-pair copulations contribute to variance in male reproductive success in the house finch (Carpodacus mexicanus), we used DNA fingerprinting to determine the paternity of chicks from 35 nests. This species is a socially monogamous passerine in which plumage brightness serves as a sexually selected indicator of male quality. Out of 119, nestlings 10 (8.3%) were fathered by a male other than the attending male, but cuckoldry occurred randomly with respect to the plumage colouration, size, or age of the attending male. Thus extra-pair fertilizations do not generate variance in male reproductive success with respect to plumage colour. On the other hand, a strongly male-biased sex ratio and asynchronous breeding by females may generate substantial variance in male reproductive success and could explain the evolution of ornamental colouration.     

Parasite distribution and virulence: implications for parasite-mediated sexual selection

The Hamilton-Zuk hypothesis states that females choosing males with more developed secondary sexual traits, i.e. brighter males, achieve greater fitness if variability in brightness reflects heritable variation in resistance to parasites. However, several factors will affect the likelihood that parasites play a role in sexual selection in given species. Here, using simple models, we show that because of parasite aggregation on a few hosts, only few breeding males would suffer from reductions in brightness due to parasites. Only in cases where parasites are abundant and show low levels of aggregation among their hosts would there be sufficient variability in brightness among breeding males for female choice of bright, resistant males to evolve. In addition, sufficient parasite-induced variability in brightness among breeding males will only occur in host-parasite systems where pathology is linearly related to the number of parasites per host. The presence of males that are uninfected and bright but genetically susceptible to parasites will also influence the fitness advantages obtained by females choosing bright males. If genetic immunity against parasites is rare in the host population, females can probably only benefit from choosing bright males if parasites are common and little aggregated among males. These results greatly limit the generality of the Hamilton-Zuk hypothesis, and suggest that only a small fraction of host-parasite associations could promote the evolution of host mate choice for resistance based on brightness. Correspondence to: R. Poulin     

Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection

Life-history theory predicts that individuals should increase their reproductive effort when the fitness return from reproduction is high. Females mated with high-quality males are therefore expected to have higher investment than females mated with low-quality males, which could bias estimates of paternal effects. Investigating the traits females use in their allocation decisions and the aspects of reproduction that are altered is essential for understanding how sexual selection is affected. We studied the potential for differential female allocation in a captive population of a precocial bird, the Chinese quail, Coturnix chinensis. Females paired with males with large sexual ornaments laid larger, but not more, eggs than females paired with males with small sexual ornaments. Furthermore, female egg mass was also significantly positively affected by male testis size, probably via some unknown effect of testis size on male phenotype. Testis size and ornament size were not correlated. Thus, both primary and secondary male sexual traits could be important components of female allocation decisions. Experimental manipulation of hormone levels during embryonic development showed that both male and female traits influencing female egg size were sensitive to early hormone exposure. Differences in prenatal hormone exposure as a result of maternal steroid allocation to eggs may explain some of the variation in reproductive success among individuals, with important implications for non-genetic transgenerational effects in sexual selection.Communicated by C. Brown     

Limb regeneration and subsequent asymmetry in a male secondary sexual character influences sexual selection in wolf spiders

Males of the brush-legged wolf spider Schizocosa ocreata (Hentz) have conspicuously decorated forelegs used in courtship and agonistic displays. Approximately one in five juvenile males has a missing or regenerating foreleg, and regeneration of a leg lost during development usually results in the absence of a decorative tuft on that leg. The subsequent asymmetry in this male secondary character significantly decreases success in both courtship of females and male-male agonistic interactions. Experimental removal of tufts from one leg of previously successful symmetric males produces similar results. As a test for concomitant behavioral effects, female spiders were shown video images of a courting male with symmetric tufts and the same video image altered to have asymmetric tufts. Female receptivity to the asymmetric video image was lower. In contrast to fluctuating asymmetry resulting from developmental instability, leg tuft asymmetry in S. ocreata most likely arises from a single event during ontogeny – possibly leg loss from an aggressive or predator encounter  – and may serve as a quality indicator in female mate choice. Received: 27 July 1995/ Accepted after revision: 19 November 1995     

Female preference and sexual selection for male coloration in the guppy (Poecilia reticulata)

Summary Experiments were designed to determine the effects of male pigmentation patterns on female choice in guppies. When presented with a series of variably-colored males, females of different genetic strain consistently exhibited similar preferences (Tables 1 and 2), preferring those males with the greatest development of both carotenoid and iridescent pigments (Table 3). A partial rank correlation analysis of pigments of males indicates positive correlations between the iridescent and carotenoid pigments and also between melanins and showiness (Table 4). Only when either the carotenoid or iridescent pigments were held constant was there any effect of the other pigments on the ranking order of males by the females. Other pigments appear to be relatively unimportant in influencing female choice of males. These results indicate that females discriminate among males on the basis of color and that females of different strains prefer the same male colors rather than those characteristics of males of their own strain. The results support those models of sexual selection that hold that sexually selected traits honestly advertise the phenotypic and genetic qualities of males; they do not support models of runaway selection for particular male traits, such as first proposed by Fisher (1930).     

Rhythmic male reproductive behavior controls timing of courtship and mating in Laupala cerasina

In many organisms, mating behavior occurs at a particular time of day, which may be important for avoiding mate competition or interspecific mating. Crickets of the Hawaiian genus Laupala exhibit an unusually protracted courtship in which males produce a series of nuptial gifts prior to the species-typical time of mating. Mating time is one of several rhythmic behaviors that have diverged among closely related Laupala species, which exhibit an extremely high speciation rate. Mating rhythm may reflect direct selection on male and/or female sexual receptivity or the pleiotropic consequence of selection on other rhythmic behaviors. To examine the role of sexual rhythmicity in Laupala cerasina, we characterized the time boundaries or “circadian gate” of courtship and mating, as well as female phonotactic response to male song. We also examined which sex is responsible for mating rhythmicity by phase-shifting males relative to the female photophase. Our results demonstrate that mating behavior is gated by the end of the light phase. Time limits to female mating receptivity were not observed and thus male rhythm alone appears to be responsible for the timing of mating. Furthermore, when courtship is initiated later in the day, males produce fewer nuptial gifts and increase nuptial gift production rate while delaying mating, suggesting that the number of gifts a female receives is important to male reproductive success.     

Bumblebees as model organisms to study male sexual selection in social insects

Social-insect males are often regarded as being merely short-lived "flying sperm containers", which ignores their potential influence on females and paternity patterns as found in other animals. Consequently, social-insect males have received only marginal attention and sexual selection has almost never been studied in these species. Here I present a review of the mating biology of bumblebees (Bombus spp.), which are the best-studied social insects to date. I follow a male's pathway from his birth until he successfully contributes to the next generation, and show that males have evolved adaptations and behaviors to influence paternity patterns at various stages of their life, which are similar to those exhibited by males of non-social insects. By comparing the available bumblebee data with more sparse studies of male reproductive behavior in other social Hymenoptera, I argue that such male adaptations may indeed be widespread in social insects. I suggest that current paradigms on sexual selection should be challenged by using social insects as model systems, because they offer unique features, and a solid theoretical background in which clear predictions can be made and appropriate experimental tests of them can be designed.Communicated by A. Cockburn     

Mate choice in the yellow-shouldered widowbird: correlates of male attractiveness

Recent investigations of male ornaments in sexual selection have used experimental manipulation of tail length in three widowbird species, but only for one of these have correlates of male reproductive success been reported. I examined correlates of male attractiveness to nesting females over two breeding seasons for the polygynous yellow-shouldered widowbird, Euplectes macrourus, in order to discover which cues females may be using to select mates. The black, long-tailed ( 10 cm) males defend large territories and build nest frames, or cock's nests, which females then line and use for nesting. I examined various aspects of male morphology, five behavioral displays, territory characteristics, and the number of cock's nests that males built. Few correlates of mating success were found. The best predictor was the number of cock's nests that a male builds, though one courtship display also correlated with male mating success in 1 year, as did average grass height. Tail length did not correlate with male mating success. A partial correlation analysis confirmed that cock's nests and, in 1 year, grass height, were the primary contributers to male success. Females may choose where to nest primarily on the availability of suitable nesting sites. Long tails may be used by females seeking extra-pair copulations or in male-male competition for territories.     

Condition dependence of sexual attractiveness in the bank vole

The capture of genetic variation by sexual traits due to their condition dependence is hypothesized to underlie the genetic benefits of mate choice. Here, we investigate condition dependence of sexual attractiveness of bank vole Myodes glareolus males by manipulating their diet during the period of maturation. We find that reducing diet quality negatively affected both male mating success and development of preputial glands used in sexual signaling. Preputial glands showed stronger condition dependence than other organs measured (testes, heart, intestines). In contrast to mating success, male dominance was not significantly affected by diet manipulation and was not correlated with male mating success. Thus, our results support condition dependence of sexual attractiveness but not of intrasexual competitiveness.     

Male signaling behavior and sexual selection in a wolf spider (Araneae: Lycosidae): a test for dual functions

Male signaling behaviors are often studied in a single context but may serve multiple functions (e.g., in male–male competition and female mate choice). We examined the issue of dual function male signals in a wolf spider species Schizocosa ocreata (Hentz) that displays the same species-specific signaling behaviors in both male–male and male–female contexts. These signaling behaviors have been described as either aggression or courtship according to the context observed. We tested the possibility of dual functions by comparing the relationship between behaviors and outcome of male–male contests (winner/loser) and male–female mating encounters (mating success). Frequency, rate, and mean duration of signaling behaviors did not vary with outcome of male–male contests, which appears instead to be based upon relative size and body mass. Winners of contests had significantly greater body mass than losers, and greater mass relative to opponents was significantly associated with probability of winning. Overall, signaling rates were much higher in male–female interactions than in male–male contests and were higher for males that successfully mated than for those that did not mate. Mean duration of some male displays was also greater for males that successfully mated. However, male size was not associated with probability of mating. Taken together, results suggest an intersexual selection context for the current function of male signals in these wolf spiders and that increased display vigor is associated with male mating success.     

An ultraviolet signal generates a conflict between sexual selection and species recognition in a newt

Whether sexual selection and species recognition involve distinct preferences and signals is still debated. Earlier work showed that traits under sexual selection can reduce the efficiency of species recognition but remains uncertain on how frequently such a conflict occurs. We can, however, hypothesise that overlapping distributions of sexual signals may enhance the hybridization risk in many species. We tested this hypothesis in a newt, Lissotriton vulgaris, which hybridises with Lissotriton helveticus. The two species also share an ultraviolet (UV) colour trait, which influences male attractiveness in L. vulgaris, though this trait is probably not functional for sexual communication in L. helveticus. We predicted that the shared trait would affect species recognition when UV radiation is present in the environment. We staged binary choice preference tests under UV+ and UV? conditions. In the UV+ treatment, female preference depended on the values of the shared UV trait and total brightness, regardless of male species identity. Thus, species recognition was enhanced or reversed depending on the difference in the male trait. Females preferred no male type in the UV? treatment, likely explained by our design, which alternated different sensory environments, and the limited prior exposure of subjects to the other species’ morph. We conclude that the presence of this shared trait used in sexual communication contributes to the production of hybrids in syntopic ponds. To our knowledge, this is the first experimental evidence of the influence of an UV sexual signal modulating species recognition.     

Sympatric sexual signal divergence among North American Calopteryx damselflies is correlated with increased intra- and interspecific male–male aggression

Divergence of sexual signals in sympatry can arise as a consequence of (1) interspecific competition for resources, (2) selection against maladaptive hybridization, or (3) as a result of selection to reduce the cost of interspecific aggression; termed agonistic character displacement (ACD). Calopterygid damselflies have emerged as a model system for studying the evolution of divergent sexual signals due to the repeated evolution of sympatric species pairs with fully and partially melanized wings. Damselfly wing patterns function during both courtship and territory defense. However, the relative contributions of natural and sexual selection to phenotypic divergence and enhanced isolation in sympatry remain unclear in many cases. Here, we investigated the hypothesis that interference competition, in the form of increased interspecific male–male aggression, drives the evolution of character displacement in sympatry between two species of North American damselflies, Calopteryx aequabilis and Calopteryx maculata, that show no evidence of ecological divergence or ongoing hybridization. In paired behavioral trials, we found that interspecific male aggression related to territory defense varied between site, species, and as a function of the relative abundance of con- vs. hetero-specific males. Specifically, we found that large-spotted C. aequabilis males received increased intra- and interspecific aggression but that aggression against large-spotted males declined during the middle of the flight season when both species were equally abundant. Based on these results, we suggest that ACD leads to enhanced species recognition, and may be a common outcome of the antagonism between interspecific male–male competition and the countervailing force of intraspecific sexual selection favoring increased wing melanization among territorial damselfly species.     

Swarming and mating behavior of a mayfly Baetis bicaudatus suggest stabilizing selection for male body size

Large size often confers a fitness advantage to female insects because fecundity increases with body size. However, the fitness benefits of large size for male insects are less clear. We investigated the mating behavior of the mayfly Baetis bicaudatus to determine whether the probability of male mating success increased with body size. Males formed mating aggregations (swarms) ranging from a few to hundreds of individuals, 1-4 m above the ground for about 1.5-2 h in the early morning. Females that flew near swarms were grabbed by males, pairs dropped to the vegetation where they mated and then flew off individually. Some marked males returned to swarms 1, 2 or 3 days after marking. Larger males swarmed near spruce trees at the edges of meadows, but the probability of copulating was not a function of male body size (no large male advantage). Furthermore, the potential fitness advantage of mating with larger, more fecund females was not greater for large males (no size-assortative mating). However, the sizes of copulating males were significantly less variable than those of non-mating males collected at random in swarms. Intermediate male size may be optimal during mating because of trade-offs between flight agility and longevity or competitive ability. Results of this study are consistent with the hypotheses that there is stabilizing selection on adult male body size during mating, and that male body size in this species may be influenced more by selection pressures acting on larvae than on adults.     

Mating in the red-sided garter snake,Thamnophis sirtalis parietalis: differential effects on male and female sexual behavior

Summary Female red-sided garter snakes, Thamnophis sirtalis parietalis, become unattractive to most males after mating in the field and in the laboratory. Male red-sided garter snakes vary in their latencies to court attractive females following copulation, with courtship resuming in minutes to hours. Unsuccessful males in mating balls disperse from mating pairs, but are not residually inhibited from courting attractive females. These patterns of behavior indicate that males have evolved mechanisms to maximize opportunities for copulation with several females, while females mate only once per season.     

Female distribution affects mate searching and sexual selection in male northern water snakes (Nerodia sipedon)

Mating systems and sexual selection are assumed to be affected by the distribution of critical resources. We use observations of 312 mating aggregations to compare mate-searching success of male northern water snakes (Nerodia sipedon) in two marshes in which differences in mating substrate availability resulted in more than fourfold differences in female dispersion. Reproductive males had significantly larger home ranges where females were dispersed than where females were clumped. The number of females encountered by males increased significantly with male home range size where females were dispersed, and decreased significantly where females were clumped. Where females were clumped, males were more likely to encounter other males when they located females. We found no evidence in either population that mate searching was energetically expensive or that males with relatively more energy had larger home ranges. However, males with greater fat reserves at the start of the season participated in more mating aggregations when females were dispersed, suggesting that fat reserves could affect a male’s willingness to attempt mating or to persist in aggregations. When females were dispersed there was weak stabilizing selection acting to maintain male body size (β=–0.14), but strong directional selection favoring larger (β=0.50) and fatter (β=0.37) males. Over 7 years, the intensity of selection favoring larger males varied substantially (β=0.14–1.15), but that variation was not related to variation in the operational sex ratio. We found no evidence of directional selection on either body size (β=0.05) or fat reserves (β=0.10) of males when females were spatially clumped. Overall, the distribution of females had a pronounced effect on male behavior, on the factors that affected male success in locating females, and probably on the extent of sperm competition once females had been located. Received: 23 November 1998 / Received in revised form: 9 August 1999 / Accepted: 18 August 1999     

Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds

Pinnipedia contains some of the most spectacular examples of sexual size dimorphism, examples that are therefore frequently used to illustrate the theory of sexual selection. This paper addresses the question of whether a significant relationship between sexual selection and size dimorphism exists in a comparative context. Thus, harem size and body size data gathered from the literature were analysed with independent contrasts analyses. These investigations showed that sexual size dimorphism is not a consequence of an allometric relationship between male and female size. Instead, there is a clear relationship between harem size and sexual size dimorphism. Further analyses also revealed a significant relationship between harem size and male size whereas no such relationship existed for females. These results support the hypothesis that sexual size dimorphism in pinnipeds is the product of an exclusively male response to sexual selection.     

Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird

A salient feature of many secondary sexual characteristics in animals is that their expression is controlled by sex-steroid hormones. However, for only a few types of ornaments do we know the precise molecular mechanism by which androgens like testosterone (T) enhance trait production. We studied the red carotenoid-based beak of male zebra finches (Taeniopygia guttata), which serves as a sexually selected trait and is thought to be T dependent. In previous research, we demonstrated that the extent to which male finches produce lipoproteins in the bloodstream, which bind carotenoid pigments acquired from the diet and transport them to peripheral tissues, regulates the accumulation of carotenoids in the body and beak pigmentation. Here we show that T acts to upregulate lipoprotein production and allows male zebra finches to display flashy, sexually attractive coloration. Levels of circulating T in blood positively and significantly predicted lipoprotein profile (as measured by cholesterol levels), blood carotenoid concentration, and beak color. Exogenous T administration elevated cholesterol and carotenoid status as well as beak redness. Last, experimental inhibition of T (using the anti-androgen flutamide) downregulated lipoprotein production and carotenoid circulation and faded the beak. This androgen- and lipoprotein-mediated system represents one of the more detailed physiological mechanisms underlying the development of a sex-steroid-dependent trait in animals.     

Interpopulational differences in chemical composition and chemosensory recognition of femoral gland secretions of male lizards Podarcis hispanica: implications for sexual isolation in a species complex

Summary. Molecular studies suggest that the Iberian wall lizard, Podarcis hispanica, forms a species complex with several monophyletic types. In Central Spain two of these types are spatially not isolated and may interact. Sex pheromones are important for species recognition and, thus, differences between lizards’ types in chemicals used in intraspecific communication could lead to reproductive isolation. Analyses by GC-MS showed that the femoral gland secretions of adult males of different types were different. Males of one type had twelve exclusive compounds, and proportions of some shared compounds differed. This presumably would reflect selection for the persistency and efficiency of chemical signals in different environments; less volatile compounds and with a higher chemical stability being favoured in the type of lizards inhabiting more humid climatic conditions. Differential tongue-flick rates to scents from femoral secretions indicated that males were able to detect and discriminate between males of different types based on chemical cues alone. In contrast, females detected but did not seem able to discriminate between scents of the two types of males. Thus, multiple factors might be simultaneously acting either against or in favor of speciation, leading, on the one hand, to genetic differences between types, but, on the other hand, probably precluding an effective reproductive isolation in areas where both types of lizards may interact.     

Body size and sexual selection in the koala

Sexual selection is often characterized by polygynous breeding systems, size dimorphism, and skewed operational sex ratios. Koalas are sexually dimorphic in multiple domains, yet are absent from the literature on sexual selection and the structure of their mating system is unclear. We provide the first documentation of the strength of sexual selection in koalas by using microsatellite markers to identify sires. We combine the genetic data with morphological data in order to assess the role of body size in regulating reproductive output. During our 4-year study, 37% of males were identified as possible sires. Males were significantly larger than females, with sires heavier than non-sires. Male body mass correlated with annual reproductive output, with Crow’s Index of Opportunity for Selection revealing that variation in male reproductive success was threefold higher than that of females. Since it appears that male koalas rarely engage in physical confrontations over access to females, size dimorphism could be based upon non-agonistic competition and/or female mate choice. We propose that size dimorphism in koalas evolved as a consequence of endurance rivalry promoting vocal sexual advertisements that attract females. We suggest that female choice is a key mediator of male reproductive output.