Sexual selection on alleles that determine body size in the swordtail Xiphophorus nigrensis

Summary In a natural population, we document changes in the frequencies of alleles influencing body size and size-correlated alternative male reproductive tactics, and we examine the possible role of sexual selection in producing these changes. Male swordtails (Xiphophorus nigrensis, Rio Choy) exhibit three body size classes (small, intermediate, and large) that primarily derive from allelic variation (s, I, L) at the Y-linked pituitary (P) locus. Some XX individuals are male. They are small and can be fathered either by XX or XY males. We compared the frequencies of Y-linked P alleles across two generations in a natural population. There was a significant decrease in the Y-s genotype relative to Y-I and Y-L genotypes. Laboratory experiments suggest that the disadvantage of Y-s resulted, at least in part, from female preference for larger courting males relative to small chasing males. All larger courting males are of the Y-I or Y-L genotypes. Although the frequency of Y-linked P alleles changed across generations, there was no change in the distribution of male body size classes. The stability of the phenotypic distribution across generations, despite changes in P allele frequencies, was maintained by the production of small XX sons by Y-I and Y-L males. Offprint requests to: M.J. Ryan     

“Alternative” mating behavior in the swordtails Xiphophorus nigrensis and Xiphophorus pygmaeus (Pisces: Poeciliidae)

Summary The swordtail Xiphophorus nigrensis exhibits three relatively discrete male body-size classes that derive from allelic variation at the Y-linked pituitary (P) locus. Previous studies have shown that larger males have greater relative reproductive success, and that females prefer large males. We describe the mating behavior utilized by males of each size class during individual encounters with females. Small males rely on chase behavior, similar to the alternative mating behavior classified as sneaker in small males of other species. Large males court and intermediate-sized males court or chase, depending on their body size. There is a strong correlation between P alleles for small size (s) and large size (L) with chasing and courting, respectively. The relationship between mating behavior of males of the genotype I is ambiguous. In the closely related species X. pygmaeus, males are of size similar to smaller X. nigrensis males. Paradoxically, these males do not show the courtship display that typifies larger male X. nigrensis and many other species of swordtails, but instead often employ chase behavior identical to the alternative mating behavior in small male X. nigrensis. We suggest that historical and genetic constraints, in addition to current selection forces, might be important factors in explaining the existence of alternative mating behavior in X. pygmaeus.     

Assessment and individual recognition of opponents in the pygmy swordtails Xiphophorus nigrensis and X. multilineatus

We examined factors that determine the outcome of agonistic encounters between male pygmy swordtail fish. Xiphophorus nigrensis and X. multilineatus males formed dominance relationships based on body size in staged laboratory encounters. There was a significant negative correlation between size asymmetry and fight intensity, suggesting that males assessed size in the encounters. However, a significant proportion of the variation in fight intensity in contests that escalated to bites could not be explained by size asymmetry. Aggressive motivation may also influence the outcome of contests and could be assessed in agonistic encounters. Theory suggests that signals of aggressive intention will be evolutionarily stable if individuals can recognize opponents and encounter one another repeatedly. In addition, individual recognition is one way that dominance hierarchies can be maintained. Here we demonstrate that males from both species can recognize individuals. In addition, at least some X. nigrensis males were site-faithful in the field, suggesting males encounter the same opponents repeatedly.Communicated by G.M. Klump     

Multiple paternity in a wild population of northern water snakes,Nerodia sipedon

Summary For most animal species, a single mating is sufficient to fertilize all of a female's offspring. As a result, females do not usually increase their reproductive success with successive matings. However, multiple paternity has been discovered in many animal taxa. We demonstrate that the majority of female water snakes in a wild population mate with more than one male for each litter. Field observations indicated that a highly skewed operational sex ratio (3.6:1 M : F) during the breeding season, while not necessary for multiple paternity to occur, created ample opportunity for females to mate multiply. Protein electrophoretic analysis showed that at least 12 of 14 litters from naturally mated females had more than one father. Since male snakes can not force copulations, multiple matings seem likely to be the result of female choice. Offprint requests to: F.E. Barry     

Sexual selection and species recognition in the pygmy swordtail, Xiphophorus pygmaeus: conflicting preferences

Sexual selection and species recognition play important roles in mate choice; however, sexual selection preferences may overlap with traits found in heterospecifics, producing a conflict between sexual selection and species recognition. We examined female preferences in Xiphophorus pygmaeus for male traits that could provide both types of information to determine how females use multiple cues when preferences for these cues would conflict. We also examined X. pygmaeus behavior in the field to determine if females have the opportunity to choose mates. As no male-male competition was observed in the field, and females occasionally chased males from feeding areas, females apparently have the opportunity to exercise mate choice in their natural habitat. In the laboratory, female X. pygmaeus used body size as a sexual selection cue, preferring large heterospecifics (X. cortezi) to small conspecifics. Females also preferred barless X. cortezi over barred X. cortezi when males were size matched. Because X. pygmaeus males do not have bars, this preference suggests that X. pygmaeus females use vertical bars in species recognition, and that large body size and vertical bars are conflicting cues. However, X. pygmaeus females did not have a preference for males of either species when sexual selection and species recognition cues were presented concurrently. This result was surprising, because preferences for species recognition cues are often assumed to be stronger than sexual selection cues. We suggest that females may be using additional species-specific cues in mate choice to prevent hybridization.     

Aggression and fighting ability are correlated in the swordtail fish Xiphophorus cortezi: the advantage of being barless

Males of the swordtail fish Xiphophorus cortezi are polymorphic for the pigment pattern vertical bars. Previous studies indicate that barred males exhibit higher levels of aggression towards males with bars than those without, while barless males fail to exhibit differential levels of aggression to either morph. In this study I matched barred and barless males for size and paired them in dyadic contests in order to determine if either morph was more dominant and if so, if dominance was the result of higher aggression levels. I found that barless males had higher bite frequencies and were able to win a majority of the contests while barred males consistently escalated to biting first, even though in most cases they were ultimately the losers. In order to determine whether the observed aggression levels and fighting abilities were inherent to being barless or a consequence of responses to the bars themselves, the dyads were re-paired once after barless males were given temporary bars and once after barred males had their bars removed. Thus, each morph encountered his opponent in both a barred and barless state. Regardless of bar state, naturally barless males continued to be more aggressive and more dominant than their barred counterparts. In addition, naturally barred males only won contests in which they bit more. These results indicate that for this species, aggression is an important component of winning contests when opponents are roughly the same size. As a result, naturally barless males as a whole appear to have higher resource holding potential (RHP) than naturally barred males of the same size because of their greater aggression levels.     

Unraveling the complexities of variation in female mate preference for vertical bars in the swordtail, Xiphophorus cortezi

Investigations into the nature of mate choice suggest that variation in female mate preferences is often context dependent, varying in response to genetic and environmental influences on female condition as well as to external environmental stimuli. Determining whether variation in female mate preference is adaptive requires understanding the variables involved that produce this variation and how they interact. Comparative, multivariate studies of wild-caught adult females can be used as initial assessments of variation in female mate preferences, providing valuable insights into the parameters that influence female preferences under natural conditions. We examined variation in female preferences for the pigment pattern vertical bars across five populations of the swordtail, Xiphophorus cortezi. The populations we examined are genetically differentiated and varied in the frequency of males and females with bars. We also considered a variable indicative of within-individual variation (size, as influenced by age) and a variable that varies across individuals (genotype for vertical bars: barred or barless). Using Akaike information criterion, all candidate models explaining variation in strength of preference included female bar state, female size, and population. We suggest that a combination of genetic (bar state) and environmental (female size) conditions influenced how they responded to experience with both male phenotypes in X. cortezi. Future studies should examine the possibility that barred and barless females respond differently over an environmental gradient.     

Causes and consequences of contest outcome: aggressiveness, dominance and growth in the sheepshead swordtail, Xiphophorus birchmanni

Although our understanding of how animal personality affects fitness is incomplete, one general hypothesis is that personality traits (e.g. boldness and aggressiveness) contribute to competitive ability. If so, then under resource limitation, personality differences will generate variation in life history traits crucial to fitness, like growth. Here, we test this idea using data from same-sex dyadic interaction trials of sheepshead swordtails (Xiphophorus birchmanni). In males, there was evidence of repeatable variation across a suite of agonistic contest behaviours, while repeatable opponent effects on focal behaviour were also detected. A single vector explains 80 % of the among-individual variance in multivariate phenotype and can be viewed as aggressiveness. We also find that aggressiveness predicts dominance—the repeatable tendency to win food in competition—and dominant individuals show faster post-trial weight gain (independently of initial size). In females, a dominance hierarchy predictive of weight gain was also found, but there was no evidence of variation in aggressiveness. While size often predicts contest outcome, our results show that individuals may sometimes grow larger because they are behaviourally dominant rather than vice versa. When resources are limited, personality traits such as aggression can influence growth, life history, and fitness through impacts on resource acquisition.     

Multiple paternity in wild populations of the garter snake,Thamnophis sirtalis

Summary Many adaptations have arisen in response to spern competition. In garter snakes, males produce copulatory plugs that are thought to prevent such competition. We tested this assumption using paternity exclusion techniques with electrophoretic data from 32 litters of snakes collected from two populations. Multiple paternity was confirmed in 50% of the litters examined (13/22 Michigan litters; 3/10 Wisconsin litters), and we estimate that as many as 72% of the litters may have been multiply sired. The presence of multiple paternity was also confirmed using the technique of genotypic regression. Mean relatedness in litters with evidence of multiple paternity was 0.390±0.053; in litters lacking such evidence mean relatedness was 0.498±0.022. Thus our data reveal a high incidence of multiple paternity in these snakes and suggest that their adaptations to prevent sperm competition are surprisingly ineffective.     

No evidence that sperm morphology predicts paternity success in wild house wrens

Postcopulatory sexual selection (PCSS) in internally fertilizing vertebrates is a topic of great interest, yet relatively little is known about the characteristics of sperm and ejaculates that confer an advantage in PCSS. In this study, we investigated several measures of sperm morphology that potentially contribute to fertilization success under PCSS. We tested whether sperm morphology related to success in PCSS (via extra-pair paternity) in house wrens (Troglodytes aedon). We found no evidence that sperm morphology differed between extra-pair sires and the within-pair males they cuckolded, nor that sperm morphology correlated with the proportion of within-pair offspring sired, the number of extra-pair offspring sired, or the total annual reproductive success. Male behavioral strategies may affect the probability that their sperm compete with other males’ sperm and that their sperm succeed under competition. Effects of these behavioral strategies, as well as differences between males in sperm number, could mask the effects of sperm morphology on the outcome of PCSS. Despite moderate levels of extra-pair paternity, selection on sperm may be relatively weak in house wrens. Further work is needed to understand general patterns in how sperm morphology relates to fertilization success within species.     

Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscorpion

The growing molecular evidence that females of many species mate with several males calls for a critical reassessment of the selective forces which act to shape female mating tactics. In natural populations of the harlequin-beetle-riding pseudoscorpion, Cordylochernes scorpioides, females are polyandrous and typically produce mixed-paternity broods. Laboratory behavioral analyses and breeding experiments indicate that polyandry in this pseudoscorpion is an active strategy which increases female reproductive success. Females restricted to mating with a single male experienced a higher rate of embryo failure and produced significantly fewer offspring than either females mated to more than one male in the laboratory or females naturally inseminated in the field. Forced copulation, insufficient sperm from a single mating, male nutrient donations and variation in inherent male genetic quality cannot explain the greater number of nymphs hatched by polyandrous females in this study. Evidence suggests that, by mating with several males, C. scorpioides females may exploit postcopulatory mechanisms for reducing the risk and/or cost of embryo failure resulting from fertilization by genetically incompatible sperm. Received: 5 May 1996 / Accepted after revision: 16 October 1996     

Female control of offspring paternity in a western population of red-winged blackbirds (Agelaius phoeniceus)

Extra-pair copulations, which occur when individuals that have formed social relationships to breed copulate outside their pairbond, now are recognized as an important component of reproductive success in many species. In situations where both males and females benefit from extra-pair copulations without incurring much risk, an inevitable conflict arises between pairbonded mates. In this study I investigated the conflict of interest between male and female reproductive strategies in a western population of red-winged blackbirds (Agelaius phoeniceus). Female red wings in this population initiate extra-pair copulations, which resulted in a 35% rate of extra-pair fertilization. Females initiated the majority (78%) of extra-pair copulations away from their nesting territory where pairbonded individuals typically copulate, and females that engaged in extra-pair copulations spent a significantly greater amount of time off the marsh during peak fertilization compared to females that did not. In addition, females that nested in areas with a large number of potential extra-pair partners produced significantly more extra-pair fertilized young compared to females that nested on marshes with few male neighbors. Males’ strategies to protect paternity were limited primarily to patrolling territory boundaries and to opportunistically preventing extra-pair copulations off the marsh when they were visible. In this population females appear to use behavioral means to control nestling paternity, which in turn directly affected their mate’s reproductive success, and males were restricted to using strategies that were largely ineffective at preventing the threat of extra-pair paternity. Received: 23 December 1994/Accepted after revision: 17 December 1995     

Multiple paternity and extra-group fertilizations in a natural population of California grunion (Leuresthes tenuis), a beach-spawning marine fish

Although individuals in many fish species move to shallow waters to spawn, the California grunion (Leuresthes tenuis) is almost unique in its constitutive display of synchronous full-emergence beach spawning. During a spawning event, fish ride large waves onshore to spawn on beach land, where their eggs incubate terrestrially. Here, we employ molecular markers to ascertain how this unusual reproductive behavior impacts genetic parentage. We developed and utilized four highly polymorphic microsatellite markers to assess maternal and paternal contributions in a total of 682 progeny from 17 nests of a natural population of L. tenuis. Alleles deduced to be of paternal origin in progeny were used to determine the minimum number of sires per nest and to estimate the true number of sires per nest via Bayesian analysis. We document the following: (a) no instances of multiple maternity for progeny within a nest; (b) a high frequency of nests (88%) with multiple paternity; and (c) an appreciable fraction of nests (18%) in which the estimated number of genetic sires (as many as nine) proved to be greater than the observed number of male attendants, thus implicating occasional extra-group fertilization events. From these and other observations, we also conclude that spawning behavior in grunions may involve site choice but not explicit mate choice. In addition to providing the first analysis of molecular parentage in a beach-spawning fish, we compare our findings to those reported previously for a beach-spawning arthropod, and we discuss the forces that may be maintaining this peculiar reproductive behavior.     

Digit ratios have poor indicator value in a wild bird population

Early androgen exposure is known to have long-lasting effects on phenotype, behaviour and even fitness, but difficulties in measuring the exposure hinders the study of its importance in evolutionary context. Digit ratios have been highlighted as a potential easy-to-measure indicator of early steroid exposure, as they have been suggested to reflect steroid, mainly testosterone levels during prenatal development. However, evidence for digit ratios reflecting early steroid levels is weak, as experimental studies, especially in wild populations, are scarce. We studied the association between maternally derived yolk androgens and digit ratios (2D:4D, 2D:3D and 3D:4D) using both correlative data and a rather high level of experimental elevation of yolk androgens in a passerine bird, the pied flycatcher (Ficedula hypoleuca). We also examined whether digit ratios have indicator value in an evolutionary context by studying correlations between digit ratios and reproductive traits, secondary sexual traits and exploratory behaviour. We did not find any association between digit ratios and yolk androgen level either in correlative or experimental data. Digit ratios were neither related to any of the reproductive and secondary sexual traits or exploratory behaviour measured. There was, however, a sex difference in 2D:3D and 3D:4D of adult birds (due to second and fourth digits being shorter in females), which was not apparent in fledglings or captivity-raised juveniles. This suggests that either the sex difference may develop as late as during the sexual maturation for breeding. These results indicate that, in this species, digit ratios are not reliable markers of maternally derived yolk androgen exposure and that they bear little relevance as correlates of the adaptive traits we measured.     

Polyandry in the genus Apis, particularly Apis andreniformis

Using four polymorphic microsatellite loci, we found that four Apis andreniformis queens collected in Thailand each mated at least 10–20 times, producing an average relatedness, g _ww, of workers of 0.30 ± 0.007, and an average effective number of matings of 9.1 ± 2.2. The degrees of polyandry and intra-colonial genetic relatedness in A. andreniformis are similar to those in A. mellifera, slightly more than in A. florea, and up to 6 times less than in A. dorsata. We argue that while presently favoured hypotheses for the evolution of polyandry in monogynous social insects may adequately explain the evolution of up to five or six matings, they are inadequate to explain the extreme polyandry (10–60 matings) observed in Apis. One alternative possibility is that colony fitness is a non-additive function of the fitness of individual subfamilies. Such behavioral over-dominance may mean that queen fitness is increased by high levels of polyandry, which increase the probability of desirable combinations of worker genotypes occurring in one colony. The special attributes of honey bees which may lead to behavioral over-dominance include colony aggregation (which may increase the incidence of disease), and frequent long-distance migration. Received: 8 May 1996/Accepted after revision: 9 August 1996     

Growth rates in a wild primate population: ecological influences and maternal effects

Growth rate is a life-history trait often linked to various fitness components, including survival, age of first reproduction, and fecundity. Here we present an analysis of growth-rate variability in a wild population of savannah baboons (Papio cynocephalus). We found that relative juvenile size was a stable individual trait during the juvenile period: individuals generally remained consistently large-for-age or small-for-age throughout development. Resource availability, which varied greatly in the study population (between completely wild-foraging and partially food-enhanced social groups), had major effects on growth. Sexual maturity was accelerated for animals in the food-enhanced foraging condition, and the extent and ontogeny of sexual dimorphism differed with resource availability. Maternal characteristics also had significant effects on growth. Under both foraging conditions, females of high dominance rank and multiparous females had relatively large-for-age juveniles. Large relative juvenile size predicted earlier age of sexual maturation for both males and females in the wild-feeding condition. This confirmed that maternal effects were pervasive and contributed to differences among individuals in fitness components.Communicated by J. Setchell     

Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata,revealed by DNA fingerprinting

Summary The frequency of extra-pair parentage in a wild population of zebra finches Taeniopygia guttata was examined by DNA fingerprinting. A total of 25 families, comprising 16 pairs of parents and 92 offspring (in broods of 1 to 6) were examined. Ten cases of extra-pair parentage, presumed to constitute intraspecific brood parasitism, were detected (10.9% of offspring or 36% of broods), including one possible instance of quasi-parasitism (parasitism by a female fertilized by the male nest owner). The average number of parasitic eggs per clutch detected by fingerprinting was 1.10±0.32 SD, very similar to the one egg difference in average clutch size between parasitised (6.0±0.82) and unparasitised nests (5.0±0.95). Two cases of extra-pair paternity (EPP) were detected among 82 offspring whose maternity was confirmed: 2.4% of offspring, or 8% of broods. In both cases EPP accounted for only a single offspring within a brood. Behavioural observations show that EPP occurs through extra-pair copulation rather than rapid mate switching. The results are discussed in the light of what is known about the fertile period and sperm precedence patterns in this species. Offprint requests to: T.R. Birkhead     

Social structure and co-operative interactions in a wild population of guppies (Poecilia reticulata)

In contrast to the substantial number of theoretical papers that have examined the mechanisms by which cooperation may evolve, very few studies have investigated patterns of co-operation in natural animal populations. In the current study, we use a novel approach, social network analysis, to investigate the structure of co-operative interactions in the context of predator inspection in a wild population of guppies (Poecilia reticulata). Female guppies showed social preferences for stable partners, fulfilling a key assumption made by models of reciprocity. In the laboratory, wild female guppies disproportionately engaged in predator inspection with others with whom they had strong social associations. Furthermore, pairs of fish that frequently engaged in predator inspection did so in a particularly co-operative way, potentially reducing costs associated with predator inspection. Taken together, these results provide evidence for assortative interactions forming the basis of co-operation during predator inspection in a natural fish population. The occurrence of highly interconnected social networks between stable partners suggests the existence of co-operation networks in free-ranging populations of the guppy.     

Tutor choice and imitation accuracy during song learning in a wild population of the Puget Sound white-crowned sparrow

Songbirds learn to sing by modeling their songs on the songs of other males through a process of social learning. Models of social learning predict that animals should be selective in what and when they learn. In this study, we asked whether young males in a wild population of the Puget Sound white-crowned sparrow, Zonotrichia leucophrys pugetensis, were selective in their choice of tutor models and what factors influenced how accurately they imitated tutors’ songs. We first examined two strategies for tutor choice: whether pupils have a conformity bias and/or a preference for high-quality tutors. In keeping with a conformity bias, tutors that sang song types that were relatively common within a radius of about 500 m of their territory were more likely to be imitated than were tutors that sang rarer song types. Most potential tutors were not imitated by pupils. Aspects of tutor quality, such as age, pairing status, and survival to the next year had no effect on whether a tutor’s song was imitated. Secondly, we tested whether pupil repertoire size, pupil quality, and local abundance of tutor models affected the accuracy of song imitations. We found a trade-off between repertoire size and tutor imitation accuracy with males that sang two or more song types developing significantly poorer imitations than males that sang one type. We discuss possible functions of a conformity learning strategy and factors that could produce a trade-off between imitation accuracy and repertoire size.