How do we decide that a species is sex-role reversed?

Defining sex roles has been driven by differences in mating systems at the extreme: polygyny and polyandry. Roles may reverse depending on which sex limits the reproductive rate of the other, and it is generally the female that limits the male. Males therefore compete for female mates. But in species in which the male limits the reproductive rate of the female, the female competes for male mates and assumes the masculine role. Complications arise, however, in species with typical roles when males are temporarily limiting, and females then briefly compete for and display to males. Problems also occur among tightly monogamous species with biparental care, where the mates have equal reproductive rates; both males and females compete intrasexually for mates. Despite this, monogamous species have masculine and feminine roles, typically manifested as the male dominating the female. Some monogamous species are nevertheless sex-role reversed. The pervasive behavioral mechanism characterizing the masculine role is dominance through aggression, size, or both. Attending more to behavioral mechanisms will enrich our understanding of sex-role reversal.     

Sex-role reversal is reflected in the brain of African black coucals (Centropus grillii)

In most bird species males compete over access to females and have elevated circulating androgen levels when they establish and defend a breeding territory or guard a mate. Testosterone is involved in the regulation of territorial aggression and sexual display in males. In few bird species the traditional sex-roles are reversed and females are highly aggressive and compete over access to males. Such species represent excellent models to study the hormonal modulation of aggressive behavior in females. Plasma sex steroid concentrations in sex-role reversed species follow the patterns of birds with "traditional" sex-roles. The neural mechanisms modulating endocrine secretion and hormone-behavior interactions in sex-role reversed birds are currently unknown. We investigated the sex differences in the mRNA expression of androgen receptors, estrogen receptor alpha, and aromatase in two brain nuclei involved in reproductive and aggressive behavior in the black coucal, the nucleus taeniae and the bed nucleus of the stria terminalis. In the bed nucleus there were no sex differences in the receptor or aromatase expression. In the nucleus taeniae, however, we show for the first time, that females have a higher mRNA expression of androgen receptors than males. These results suggest that the expression of agonistic and courtship behavior in females does not depend on elevated blood hormone levels, but may be regulated via increased steroid hormone sensitivity in particular target areas in the brain. Hence, aggression in females and males may indeed be modulated by the same hormones, but regulated at different levels of the neuroendocrine cascade.     

Sex-role reversal of a monogamous pipefish without higher potential reproductive rate in females

In monogamous animals, males are usually the predominant competitors for mates. However, a strictly monogamous pipefish Corythoichthys haematopterus exceptionally exhibits a reversed sex role. To understand why its sex role is reversed, we measured the adult sex ratio and the potential reproductive rate (PRR), two principal factors influencing the operational sex ratio (OSR), in a natural population of southern Japan. The adult sex ratio was biased towards females throughout the breeding season, but the PRR, which increased with water temperature, did not show sexual difference. We found that an alternative index of the OSR (Sf/Sm: sex ratio of 'time in') calculated from the monthly data was consistently biased towards females. The female-biased OSR associated with sex-role reversal has been reported in some polyandrous or promiscuous pipefish, but factors biasing the OSR differed between these pipefish and C. haematopterus. We concluded that the similar PRR between the sexes in C. haematopterus does not confer reproductive benefit of polygamous mating on either sex, resulting in strict monogamous mating, and its female-biased adult sex ratio promotes female-female competition for a mate, resulting in sex-role reversal.     

Sexual signals and mating patterns in Syngnathidae

Male pregnancy in the family Syngnathidae (pipefishes, seahorses and seadragons) predisposes males to limit female reproductive success; sexual selection may then operate more strongly on females and female sexual signals may evolve (sex-role reversal). A bewildering array of female signals has evolved in Syngnathids, e.g. skin folds, large body size, colouration, markings on the body and elaborate courtship. These female sexual signals do not seem quantitatively or qualitatively different from those that evolve in males in species with conventional sex roles where males provide females or offspring with direct benefits. In several syngnathid species, males also evolve ornaments, females are choosy in addition to being competitive and males compete as well as choosing partners. Thus, sex roles form a continuum, spanning from conventional to reversed within this group of fishes. Cases are presented here suggesting that stronger sexual selection on females may be most extreme in species showing classical polyandry (one male mates with several females, such as many species where males brood their eggs on the trunk), intermediate in polygynandrous species (males and females both mate with more than one partner, as in many species where males brood their eggs on the tail) and least extreme, even exhibiting conventional sex roles, in monogamous species (one male mates solely with one female, as in many seahorses and tropical pipefishes). At the same time caution is needed before unanimously establishing this pattern: first, the connection between mating patterns, strength of sexual selection, sex roles and ornament expression is far from simple and straightforward, and second, knowledge of the actual morphology, ecology and behaviour of most syngnathid species is scanty. Basically only a few Nerophis, Syngnathus and Hippocampus species have been studied in any detail. It is known, however, that this group of fishes exhibits a remarkable variation in sex roles and ornamentation, making them an ideal group for the study of mating patterns, sexual selection and sexually selected signals.     

Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird

In a number of insects, fishes and birds, the conventional sex roles are reversed: males are the main care provider, whereas females focus on matings. The reversal of typical sex roles is an evolutionary puzzle, because it challenges the foundations of sex roles, sexual selection and parental investment theory. Recent theoretical models predict that biased parental care may be a response to biased adult sex ratios (ASRs). However, estimating ASR is challenging in natural populations, because males and females often have different detectabilities. Here, we use demographic modelling with field data from 2101 individuals, including 579 molecularly sexed offspring, to provide evidence that ASR is strongly male biased in a polyandrous bird with male-biased care. The model predicts 6.1 times more adult males than females (ASR=0.860, proportion of males) in the Kentish plover Charadrius alexandrinus. The extreme male bias is consistent between years and concordant with experimental results showing strongly biased mating opportunity towards females. Based on these results, we conjecture that parental sex-role reversal may occur in populations that exhibit extreme male-biased ASR.     

Sex-role reversal revisited: choosy females and ornamented, competitive males in a pipefish

In the pipefish Syngnathus typhle sex roles are reversed, thatis, females compete more intensely than males over mates. However,competition over mates among individuals of one sex does notnecessarily prevent members of that same sex from being choosy,and choosiness in the other sex does not prevent competitionwithin it. In an experiment we allowed a female pipefish tochoose freely between two males, after which we released themales and let the three interact. Comparisons with earlier resultsshow that both sexes courted partners and competed with consexuals.However, females courted more often than did males, and courtshipwas more frequent in treatments involving large individualsthan in treatments with small individuals. Males competed amongthemselves for access to mates but for a shorter duration thanfemales in the same situation. Males displayed an ornament towardsfemales but not to males during mating competition. Females,however, used their ornament in both contexts. Females did notalways mate with the male of their previously made choice, whichwe interpret as females being constrained by male-male competition,male motivation to mate, or both. Thus, in this sex-role reversedspecies, mate choice in the more competitive sex may be circumventedand even overruled by mate competition and mating willingnessin the least competitive sex. Hence, sex roles should not beconsidered as sexes being either choosy or competitive but ratherthat males and females may exhibit different combinations ofchoice and competition.     

Pipefishes and seahorses: Are they all sex role reversed?

The male pregnancy of pipefishes and seahorses has led to the inference that females compete most intensely for access to mates, because males limit female reproduction. However, recent work has shown that in different species either sex may be the predominant competitor for mates. In this family, there is an apparent association between the mating pattern and the sex roles: polygamous species show reversed sex roles whereas monogamous species exhibit 'conventional' sex roles. These studies emphasize that sex role reversal is not synonymous with male parental care.     

Sex-role reversal in the tidewater goby, Eucyclogobius newberryi

Species in which females compete more intensely than males for access to mates are uncommon. Sex-role reversal in fishes has been documented only in species in which males bear eggs, such as pipefish and a mouth brooding cardinalfish. I investigated the reproductive behavior of the tidewater goby, Eucyclogobius newberryi (Gobiidae), to determine whether and to what degree this species is sex-role reversed. Males constructed and defended burrows for spawning in sand. Both sexes initiated courtship, but the female's breeding coloration was more striking. The intensity of sexual aggression was greater among females than among males. The female laid her entire clutch with a single male, and the male accepted only one clutch per brooding cycle. Both sexes spawned repeatedly (up to 12 times in aquaria), but fish did not form permanent pairs. Males cared for eggs in the burrow 9–11 days until hatching, and rarely if ever emerged to feed. Many aspects of male behavior (nest construction and defense, courtship, and parental care) were typical of most gobiids. On the other hand, female behavior (black nuptial coloration and intense female-female competition) was unusual, not only for gobiids but for animals in general. I therefore concluded that the tidewater goby is moderately sex-role reversed. Its sexual behavior is apparently unique among fishes because it is the only reported case of sex-role reversal in teleost males that do not bear eggs or developing young. This revised version was published online in July 2006 with corrections to the Cover Date.     

Should females of migratory dabbling ducks switch mates between wintering and breeding sites?

Pairing of northern hemisphere dabbling ducks normally occurs in wintering sites. Mate choice occurs when some individuals congregate in courtship parties, in which females mainly choose mates according to male behavioural dominance. The sex ratio of some species is more male-biased at northern than at southern wintering sites, and the age ratio is adult-biased in northern areas. A possible mechanism responsible for this spatial segregation of sex and age classes is behavioural dominance, with males usually dominating females and adults dominating yearlings. Due to this latitudinal segregation of sexes during winter, presumably more males would remain unpaired in northern sites utilized by the more dominant birds than in southern sites utilized by the less-dominant birds, and this is paradoxical. I argue that some females having wintered and paired in southern sites may switch mates at stopover sites during northward migration. This hypothesis provides an explanation as to why, in spite of females being paired when initiating northward migration, some species show an increase in courtship activity during spring at stopover sites, as in common teals (Anas crecca) in southern Spain. In contrast, populations that do not migrate, e.g. mallards (A. platyrhynchos) in southern Spain, do not exhibit an increase in courtship activity during spring.     

THE EVOLUTION OF REVERSED SEXUAL DIMORPHISM IN SIZE IN MONOGAMOUS SPECIES OF BIRDS

Reversed sexual dimorphism in size (RSD) occurs in most species of several taxonomic groups of birds. The hypotheses proposed to explain this phenomenon are examined theoretically, using inequalities to state selection in the most rigorous possible terms. The most pertinent empirical evidence is also examined critically. Proponents of hypotheses on the evolution of RSD have failed to consider the genetic constraints on the evolution of dimorphism. Selection for dimorphism can act on only that small portion of the genetic determination of body size that is sex limited. In general, selection for body size is much more likely to lead to a similar change (e.g. larger) in both sexes than to dimorphism. The most popular hypotheses involve selection for size-related differences in foraging ability. It is unlikely that there is variation in size-related foraging differences available for selection in a monomorphic, ancestral population. Foraging differences between the sexes cannot lead to the evolution of RSD; evolution of large and small morphs of both sexes is a more likely outcome. Selection for sex-role differentiation factors (e.g. large females lay larger eggs, small males are more agile in flight) can lead to the evolution of RSD, but only if the magnitudes of opposing selection for small males and for large females are equal. Combining selection for size-related foraging differences with selection for sex-role differentiation factors hinders the evolution of RSD until the sexes differ in size by 3 s.d . Empirical evidence supports this assertion: statistically significant differences between the sexes in the size of prey taken are found only in highly dimorphic species. The sex-role differentiation factors that have been proposed appear unlikely to provide the equal selection necessary for the evolution of RSD. Several authors have proposed that small size in males is selected for foraging ability and large size in females for some sex-role differentiation factor. Males cannot be more efficient foragers without females being less efficient and efficiency cannot be a factor only when the male is feeding his family. RSD cannot evolve in monogamous species if large females survive less well than small males. RSD might evolve as the result of sexual selection for small size in males and constraints on the reduction of size in females because of some factor associated with reproduction. Examination of seven studies indicating a relationship between female size and reproductive success shows very little unequivocal evidence for small size in females allowing breeding earlier in the season. Large size in females allows females to breed at a younger age in the sparrowhawk and pairs to form more rapidly in three species of sandpipers. Both of these may be the result of sexual selection. There are fewer theoretical problems with sexual selection as a cause for the evolution of RSD than with the other hypotheses. Empirical evidence for sexual selection is scarce but better than that for the other hypotheses. Evidence is contradictory for the selection of small size in males for agility in aerial displays for courtship or defence of territory. Large size in females does not appear to be the result of selection for competitive ability to obtain mates. Facilitation of female dominance and hence of the formation and maintenance of a pair bond is the most viable explanation of the evolution of RSD. It is most likely that all dimorphism (normal or reversed) is the result of sexual selection. RSD is correlated with birds in the diet in the Falconiformes and this is a central theme in the foraging hypotheses. This correlation may be because birds are abundant and available in a continuum of sizes, thus permitting but not causing the evolution of RSD or because species that prey upon birds are better equipped physically (and perhaps more likely behaviourally) to inflict damaging attacks on conspecifics and the greater RSD increases female dominance and the ease of pair formation.     

Breaking the rules: sex roles and genetic mating system of the pheasant coucal

Generally in birds, the classic sex roles of male competition and female choice result in females providing most offspring care while males face uncertain parentage. In less than 5% of species, however, reversed courtship sex roles lead to predominantly male care and low extra-pair paternity. These role-reversed species usually have reversed sexual size dimorphism and polyandry, confirming that sexual selection acts most strongly on the sex with the smaller parental investment and accordingly higher potential reproductive rate. We used parentage analyses and observations from three field seasons to establish the social and genetic mating system of pheasant coucals, Centropus phasianinus, a tropical nesting cuckoo, where males are much smaller than females and provide most parental care. Pheasant coucals are socially monogamous and in this study males produced about 80% of calls in the dawn chorus, implying greater male sexual competition. Despite the substantial male investments, extra-pair paternity was unusually high for a socially monogamous, duetting species. Using two or more mismatches to determine extra-pair parentage, we found that 11 of 59 young (18.6%) in 10 of 21 broods (47.6%) were not sired by their putative father. Male incubation, starting early in the laying sequence, may give the female opportunity and reason to seek these extra-pair copulations. Monogamy, rather than the polyandry and sex-role reversal typical of its congener, C. grillii, may be the result of the large territory size, which could prevent females from monopolising multiple males. The pheasant coucal’s exceptional combination of classic sex-roles and male-biased care for extra-pair young is hard to reconcile with current sexual selection theory, but may represent an intermediate stage in the evolution of polyandry or an evolutionary remnant of polyandry.     

Progesterone modulates aggression in sex-role reversed female African black coucals

Testosterone is assumed to be the key hormone related to resource-defence aggression. While this role has been confirmed mostly in the context of reproduction in male vertebrates, the effect of testosterone on the expression of resource-defence aggression in female vertebrates is not so well established. Furthermore, laboratory work suggests that progesterone inhibits aggressive behaviour in females. In this study, we investigated the hormonal changes underlying territorial aggression in free-living female African black coucals, Centropus grillii (Aves; Cuculidae). Females of this sex-role reversed polyandrous bird species should be particularly prone to be affected by testosterone because they aggressively defend territories similar to males of other species. We show, however, that territorial aggression in female black coucals is modulated by progesterone. After aggressive territorial challenges female black coucals expressed lower levels of progesterone than unchallenged territorial females and females without territories, suggesting that progesterone may suppress territorial aggression and is downregulated during aggressive encounters. Indeed, females treated with physiological concentrations of progesterone were less aggressive than females with placebo implants. This is one of the first demonstrations of a corresponding hormone-behaviour interaction under challenged and experimental conditions in free-living females. We anticipate that our observation in a sex-role reversed species may provide a more general mechanism, by which progesterone--in interaction with testosterone--may regulate resource-defence aggression in female vertebrates.     

Male mate choice, male availability and egg production as limitations on polyandry in the red-necked phalarope

In sequentially polyandrous birds, a female's second mate faces a substantial risk of cuckoldry due to rapid mate switching and stored sperm. Secondary males are potentially available to females because males arrive asynchronously and/or are recycled into the breeding pool following nest predation. In a study of red-necked phalaropes, Phalaropus lobatus, a sex-role reversed shorebird, we tested the hypotheses that the proportion of females that become polyandrous is proximately limited by: (1) the ability of females to produce eggs, (2) the availability of males as mates and (3) male mate choice. In a colour-banded population in which rates of nest loss were manipulated by researchers, females that produced second clutches required similar lengths of time to complete clutches as those contemporaneously producing first clutches, and increased their egg size relative to their first clutch, making egg limitation unlikely. There was no correlation between an annual measure of males' availability as potential mates following nest losses and the proportion of females that were polyandrous. The majority of males that lost clutches (66%) re-paired with their original female significantly more often than expected by random mate choice (P<0.0001). Although 76% of polyandrous nestings involved renesting males, only 6% (N=46) of renesting males changed mates if their original female was still available. Renesting males that changed mates did not select for or against females that had already produced clutches (NS). Our results suggest that the level of polyandry in this species is not constrained by the females' abilities to produce more eggs or by the number of males recycling back into the breeding pool. Instead, the proportion of females that become polyandrous is limited by males choosing to renest with their original females, thereby decreasing their probability of caring for eggs potentially fertilized by a female's previous mate.     

Understanding reversals in the relative strength of sexual selection on males and females: a role for sperm competition?

Sperm competition affects sexual selection intensity on males, but models suggest it cannot affect the relative intensity of sexual selection on males compared to females. However, if sperm competition depresses the payoff for male multiple mating, it could affect the relative intensity of sexual selection and even cause sexual selection to be more intense on females than males (reversal of typical pattern). To evaluate how sperm competition, energy availability, and parental investment affect the intensity of sexual selection on each sex, I constructed a simulation model using the relationship between fecundity and number of mates to estimate sexual selection gradients. Unlike earlier models, I include a trade-off between paternal investment and sperm competition ability. The amount of energy available for reproduction affects the sexual selection gradient for each sex. Reversals in the sex experiencing stronger sexual selection do occur when additional paternal investment reduces a male's ability to compete for fertilizations within females. The shape of the distribution of mates for each sex (determined by mate competition) is also important. Output from the model is qualitatively similar to empirical data from insects with paternal investment. This model challenges previous thinking about the role of sperm competition in sex-role reversal.     

Sex differences in intrasexual aggression among sex-role-reversed,cooperatively breeding cichlid fish <Emphasis Type="Italic">Julidochromis regani</Emphasis>

In sex-role-reversed species, females compete for resources (e.g., mates) more intensively than do males. However, it remains unclear whether these species exhibit sex differences in the intensity of aggressive behavior in the context of within-sex contests. Cichlid fish in the genus Julidochromis exhibit intraspecific variation in mating systems, ranging from monogamy to cooperative polyandry with sex-role reversal. In the study reported here, we observed aggressive interactions among three same-sex individuals in Julidochromis regani in the laboratory and tested whether inter-female aggression was more intense than inter-male aggression. Although difference in body size strongly determined the direction of aggression in fish, aggression by a smaller-sized individuals toward larger ones was occasionally observed. This type of aggression was common between individuals of a similar body size (≤5 mm) and occurred more frequently among females than males. In contrast, differences in body size and sex did not affect the frequency of aggression by larger-sized individuals against smaller ones. Bidirectional aggression (i.e., mouth fighting) occurred frequently when two individuals had similar body size, and there was no difference in its frequency between sexes. However, temporal analysis showed that females performed bidirectional aggression more persistently than males. These sex differences in the intensity of intrasexual aggression could be the behavioral mechanisms underpinning cooperative polyandry.     

Plasma steroid hormones in relation to behavioral sex role reversal in the spotted sandpiper, Actitis macularia

Plasma samples collected from spotted sandpipers during the reproductive season were analyzed for testosterone, dihydrotestosterone (DHT), estradiol-17 beta and progesterone. Prior to incubation, plasma testosterone and DHT levels were significantly greater in males than in females. Estradiol levels of paired females were significantly greater than those of paired males. Testosterone and DHT levels of unpaired resident and paired males were significantly greater than those of incubating and brooding males. A 25-fold decline in testosterone occurred in males from the 1- or 2-egg stage to the 3-egg stage, when incubation is initiated. In females, testosterone values were low in unpaired, brooding, and transient birds. Paired females had levels 7-fold greater than unpaired birds. In both sexes, there was a strong correlation between testosterone and DHT levels. Prolactin values were negatively correlated with testosterone and DHT in males. These results indicate that the high level of intrasexual competition for mates among female spotted sandpipers is not based upon a total reversal of the normal male/female levels of androgens and estradiol. Territoriality and intense competition for mates in females may be based upon enhanced receptivity of neural centers to moderate hormone levels. Relative changes in testosterone between unpaired and paired females indicates that this hormone may play a role in mate acquisition and territoriality of these sex role-reversed females.     

Greater opportunities for sexual selection in male than in female obligate brood parasitic birds

Females are expected to have evolved to be more discriminatory in mate choice than males as a result of greater reproductive investment into larger gametes (eggs vs. sperm). In turn, males are predicted to be more promiscuous than females, showing both a larger variance in the number of mates and a greater increase in reproductive success with more mates, yielding more intense sexual selection on males vs. females (Bateman's Paradigm). However, sex differences in costly parental care strategies can either reinforce or counteract the initial asymmetry in reproductive investment, which may be one cause for some studies failing to conform with predictions of Bateman's Paradigm. For example, in many bird species with small female‐biased initial investment but extensive biparental care, both sexes should be subject to similar strengths of sexual selection because males and females are similarly restricted in their ability to pursue additional mates. Unlike 99% of avian species, however, obligate brood parasitic birds lack any parental care in either sex, predicting a conformation to Bateman's Paradigm. Here we use microsatellite genotyping to demonstrate that in brood parasitic brown‐headed cowbirds (Molothrus ater), per capita annual reproductive success increases with the number of mates in males, but not in females. Furthermore, also as predicted, the variance of the number of mates and offspring is greater in males than in females. Thus, contrary to previous findings in this species, our results conform to predictions of the Bateman's Paradigm for taxa without parental care.     

Mating systems,philopatry and dispersal in birds and mammals

Many species of birds and mammals are faithful to their natal and breeding site or group. In most of them one sex is more philopatric than the other. In birds it is usually females which disperse more than males; in mammals it is usually males which disperse more than females. Reproductive enhancement through increased access to mates or resources and the avoidance of inbreeding are important in promoting sex differences in dispersal. It is argued that the direction of the sex bias is a consequence of the type of mating system. Philopatry will favour the evolution of cooperative traits between members of the sedentary sex. Disruptive acts will be a feature of dispersers.     

Temperature affects male and female potential reproductive rates differently in the sex-role reversed pipefish, Syngnathus typhle

The differences in potential reproductive rate between the sexescan be used to predict the operational sex ratio and the patternsand intensity of mating competition and hence sexual selectionin a population. This article describes how one environmentalcomponent, temperature, affects potential reproductive ratesof the two sexes in the paternally brooding, sex-role reversedpipefish (Syngnathus typhle). Males brooded embryos much longer(on average 58 days) in cold water (about 10°C) than inwarmer water (35 days at about 15°C). As a consequence,the potential reproductive rate (number of eggs brooded perday) of males was significantly higher in warm water. In females,however, potential reproductive rate, i.e., number of eggs producedper day given an unlimited access to mates, was not significantlydifferent between temperatures. In both sexes, potential reproductiverate was positively related to body size. At both temperatures,females had the potential to reproduce faster than males. Asa result, the operational sex ratio will become female biasedand sex-roles reversed, as is the case in this species. Sincetemperature differently influenced the potential reproductiverates of males and females, with the sexual difference largerat lower temperatures, more intense female-female competitionis predicted at low temperatures.