Competing Females and Caring Males. Polyandry and Sex-Role Reversal in African Black Coucals, Centropus grillii

Most species of birds show bi‐parental or female‐only care. However, a minority of species is polyandrous and expresses male‐only care. So far, such reversals in sex roles have been demonstrated only in precocial bird species, but there was suggestive evidence that such a mating system may occur in one altricial bird species, the black coucal, Centropus grillii. In a field study in Tanzania we investigated whether black coucals are sex‐role reversed and polyandrous. We found that males were mated to one female, rarely vocalized and provided all parental care from incubation of eggs to feeding of young. In contrast, female black coucals were about 69% heavier and 39% larger than males and polyandrous. They spent a large proportion of time calling from conspicuous perches, defended breeding territories, did not help in provisioning young and had a higher potential reproductive rate than males. We conclude that the black coucal currently represents the only altricial bird species with sole male parental care and a classical polyandrous mating system. High nest predation pressure and small territory sizes due to high food abundance may have been important factors in the evolution of sex‐role reversal and polyandry in this species.     

Social monogamy vs. polyandry: ecological factors associated with sex roles in two closely related birds within the same habitat

Why mainly males compete and females take a larger share in parental care remains an exciting question in evolutionary biology. Role‐reversed species are of particular interest, because such ‘exceptions’ help to test the rule. Using mating systems theory as a framework, we compared the reproductive ecology of the two most contrasting coucals with regard to sexual dimorphism and parental care: the black coucal with male‐only care and the biparental white‐browed coucal. Both species occur in the same lush habitat and face similar ecological conditions, but drastically differ in mating system and sexual dimorphism. Black coucals were migratory and occurred at high breeding densities. With females being obligatory polyandrous and almost twice as heavy as males, black coucals belong to the most extreme vertebrates with reversed sexual dimorphism. Higher variance in reproductive success in fiercely competing females suggests that sexual selection is stronger in females than in males. In contrast, resident white‐browed coucals bred at low densities and invariably in pairs. They were almost monomorphic and the variance in reproductive success was similar between the sexes. Black coucals were more likely to lose nests than white‐browed coucals, probably facilitating female emancipation of parental care in black coucals. We propose that a combination of high food abundance, high population density, high degree of nest loss and male bias in the adult sex ratio represent ecological conditions that facilitate role reversal and polyandry in coucals and terrestrial vertebrates in general.     

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.     

Competing females and caring males. Sex steroids in African black coucals, Centropus grillii

The black coucal is the only known altricial bird species in which females mate with and lay eggs for more than one male and males are responsible for all parental care (classical polyandry). In this species, the left testis is atrophied and it has been speculated that this may result in a reduction of circulating androgens, providing a unique mechanism for reversals in sex roles. We therefore investigated whether there is a reversal in circulating androgens and oestrogens in black coucals. Despite the reversals in sex roles, males had significantly higher levels of plasma testosterone than females, in a pattern typical of that of monogamous male passerines. Testosterone levels of both sexes were higher during the mating than during the premating stage and were low in males during the nestling stage. The concentrations of androstenedione, dehydroepiandrosterone and oestradiol did not differ between the sexes and were generally low. A physiological challenge with gonadotropin-releasing hormone (GnRH) resulted in a significant increase in testosterone in males but not in females, suggesting either that females are not responsive to GnRH or that they express patterns of testosterone that are similar to those of males of species with a polygynous mating system without paternal care, in which testosterone is expressed at maximum levels throughout the breeding season. We conclude that the absence of one testis does not provide a mechanism for sex role reversal in black coucals. Either androgens are not involved in the regulation of male-like traits in females or females are sensitive to relatively low levels of these steroids.     

Males paving the road to polyandry? Parental compensation in a monogamous nesting cuckoo and a classical polyandrous relative

Comparative studies have established the necessity for biparental care as an important factor for monogamy in freshwater fish and birds. However, whether two parents are really needed for offspring care remains an open question in many cases. I experimentally studied female and male contributions to offspring care in the white-browed coucal (Centropus superciliosus), a monogamous and biparental cuckoo with a balanced adult sex ratio, and contrasted it with the sympatric black coucal (C. grillii), a classically polyandrous species with a male-biased adult sex ratio and male-only care. To study the necessity for biparental care, I temporarily removed one partner for 2 days to see whether the remaining parent compensated for the absence of its partner. Both female and male white-browed coucals approximately doubled their feeding rates when their partner was absent, thus fully compensating the number of feeding visits to the nest. However, nestlings maintained their growth only, when males were present and females were removed. When males were removed and only females were present, nestling growth declined. Hence, only male white-browed coucals fully compensated for the temporary loss of the partner, suggesting that females could benefit most from nesting with additional males—if these should become available. Removing female black coucals had no consequence for nestling feeding rates of male black coucals. But male black coucals had to be returned to their territories within a few hours to avoid harming the brood because female black coucals typically would not commence feeding their offspring. In conclusion, the breeding system of white-browed coucals seems quite flexible and the relatively balanced adult sex ratio may stabilize monogamy in this species. Should ecological factors ever favour a stronger bias in the adult sex ratio towards males, female white-browed coucals may easily become polyandrous and relinquish parental care entirely to males.     

Evolution of reversed sex roles, sexual size dimorphism, and mating system in coucals (Centropodidae, Aves)

The evolution of greater male than female parental care remains poorly understood. In birds it is thought to be related to precocial chicks and small clutch size. This review shows, however, that such role reversal has also evolved in a family with altricial young and relatively large clutch size: coucals (Centropodidae, Cuculiformes). Males perform most nest building, incubation, and feeding of young. As predicted by sexual selection theory, coucals have also reversed sexual size dimorphism, females being larger than males in all 12 species for which size data are available. Most coucals that have been studied are monogamous, but the black coucal Centropus grillii appears to be polyandrous, and males perform almost all parental care, whereas females show more active advertisement behaviour. In this species, females are about 50% heavier than males. Polyandry in the black coucal seems to be associated with a shift to a habitat with seasonally rich food resources. Difficulties for female coucals of gathering enough resources for producing several clutches of relatively large eggs may favour mainly male parental care. Female sexual competition and resource storage, and male foraging economy, may explain why females are larger. Additional field studies are needed to test these hypotheses; the coucals are of great interest to sexual selection and mating systems theory.     

Evolution of Classical Polyandry: Three Steps to Female Emancipation

Abstract In classical polyandry, sex roles are reversed and a female reproduces with several males, each of whom raises his offspring with little or no help from her. This mating system occurs in some fishes and birds, and it is of great interest in relation to parental investment, sex role and sexual selection theory. The evolution of classical polyandry, however, is debated and not well understood. It is here suggested to generally take place in three main steps. (1) First evolves male care for eggs, for reasons that differ between fishes and birds. (2) Second, a female becomes able to lay more eggs than a male can accommodate. This can happen, for example, by evolution of male pregnancy or smaller body size, or by female production of more or larger eggs, made possible by larger female body size or more food. Polyandry in several taxa is associated with shift to a habitat rich in food during the breeding season, to novel specialised foraging methods, or to both. A favourable food situation may be crucial for evolution of classical polyandry. (3) In step three, females compete to lay two or more clutches in sequence for different males. Successful polyandrous females obtain more offspring, spreading traits that enhance success in competition over males. Step three may be most likely in species with small body size, for reasons of reproductive constraints and seasonality. Evolution of classical polyandry appears to have followed these steps in shorebirds, coucals and pipefishes, but the reasons why certain species differ from their close phylogenetic relatives in being polyandrous are far from clear. Behavioural and ecological studies of additional species, and detailed phylogenies of taxa with diverse mating systems including polyandry, are needed for testing these ideas.     

Polymorphic microsatellite loci in pheasant coucal (Centropus phasianinus)

Little is known about the effect of male parental care and behavioural sex‐role reversal on the mating system of birds because genetic markers for species with these characteristics are lacking. We developed primers for nine polymorphic microsatellite loci in pheasant coucals (Centropus phasianinus). Eight of the primers were also polymorphic in African black coucals (Centropus grillii). Pheasant coucals are of particular interest in the study of evolutionary and behavioural ecology, because their sex‐role reversal and extensive male parental care suggests low levels of extra‐pair fertilizations, yet they have large testes indicating sperm competition.     

Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

Polyandry in Bicyclus anynana Butterflies Results from Sexual Conflict over Mating

Although only one or just a few matings are considered sufficient to maximise a female's reproductive success, polyandry is a common mating system in insects and other animals. Female polyandry may either result from direct or indirect benefits of mating multiply, or from male harassment and thus sexual conflict over mating. Here, we test whether the latter is involved in determining female mating frequency in the butterfly Bicyclus anynana. We used a full‐factorial design with three different sex ratios and densities each, resulting in a total of nine treatment groups. Sex ratio but not density affected female mating frequency, which increased with an increasingly male‐biased sex ratio. Our results thus suggest that female polyandry in B. anynana results from sexual conflict, although females seem to be able to reject courting males at least to some extent. Therefore, polyandry in this species may occur in the first place from convenience, as the costs of resisting male harassment may be higher than mating repeatedly.     

Mortality costs of sexual selection and parental care in natural populations of birds

Abstract Is the cost of reproduction different between males and females? On the one hand, males typically compete intensely for mates, thus sexual selection theory predicts higher cost of reproduction for males in species with intense male‐male competition. On the other hand, care provisioning such as incubating the eggs and raising young may also be costly, thus parental care theory predicts higher mortality for the care‐giving sex, which is often the female. We tested both hypotheses of reproductive costs using phylogenetic comparative analyses of sex‐specific adult mortality rates of 194 bird species across 41 families. First, we show that evolutionary increases in male‐male competition were associated with male‐biased mortalities. This relationship is consistent between two measures of mating competition: social mating system and testis size. Second, as predicted by the parental cost hypothesis, females have significantly higher adult mortalities (mean ± SE, 0.364 ± 0.01) than males (0.328 ± 0.01). However, the mortality cost of parental care was only detectable in males, when the influence of mating competition was statistically controlled. Taken together, our results challenge the traditional explanation of female‐biased avian mortalities, because evolutionary changes in female care were unrelated to changes in mortality bias. The interspecific variation in avian mortality bias, as we show here, is driven by males, specifically via the costs of both mating competition and parental care. We also discuss alternative hypotheses for why most birds exhibit female‐biased mortalities, whereas in mammals male‐biased mortalities predominate.     

Sex differences in parental care: Gametic investment,sexual selection,and social environment

Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (1) differential gametic investment by males and females that precipitates into sex difference in care, (2) different intensity of sexual selection acting on males and females, and (3) biased social environment that facilitates the more common sex to provide more care. Here, we provide the most comprehensive assessment of these hypotheses using detailed parental care data from 792 bird species covering 126 families. We found no evidence for the gametic investment hypothesis: neither gamete sizes nor gamete production by males relative to females was related to sex difference in parental care. However, sexual selection correlated with parental sex roles, because the male share in care relative to female decreased with both extra‐pair paternity and frequency of male polygamy. Parental sex roles were also related to social environment, because male parental care increased with male‐biased adult sex ratios (ASRs). Taken together, our results are consistent with recent theories suggesting that gametic investment is not tied to parental sex roles, and highlight the importance of both sexual selection and ASR in influencing parental sex roles.     

Who Cares? Males Provide Most Parental Care in a Monogamous Nesting Cuckoo

Cuckoos hold a prominent position in the study of parental care, because they show the greatest variation of any bird family in the way they care for their offspring. Despite this, few data are available on cuckoos with biparental care even though it is the most common form of parental care in cuckoos and birds in general. Here I describe the breeding behaviour of the pheasant coucal, Centropus phasianinus , an old-world nesting cuckoo. I show that males almost exclusively build the nest and incubate and brood the young alone both at night and during the day. The incubation pattern of short, c . 40 min bouts on the nest interspersed with 20 min frequent recesses is well suited to incubation by a single parent and is widespread amongst birds. Males also defend the nestlings and deliver 80% of the feeds to the young consisting of insects (65%), frogs and reptiles. Females did not compensate for their fewer feeding visits by delivering more vertebrates than males. Although coucal males get little help feeding, the hourly feeding rate of 3.8 feeds per brood (1.4 feeds/nestling) exceed that of the few nesting cuckoos studied to date and matches that of other tropical non-passerines. Predominantly male care is found in less than 5% of birds, mainly species with reversed sexual size dimorphism or reversed sex-roles. Its evolution, especially in monogamous species, remains puzzling. The breeding behaviour of pheasant coucals illustrates a possible transitional stage in the evolution of polyandry and interspecific brood parasitism in cuckoos.     

Conflict over multiple-partner mating between males and females of the polygynandrous common lizards

The optimal number of mate partners for females rarely coincides with that for males, leading to a potential sexual conflict over multiple-partner mating. This suggests that the population sex ratio may affect multiple-partner mating and thus multiple paternity. We investigate the relationship between multiple paternity and the population sex ratio in the polygynandrous common lizard (Lacerta vivipara). In six populations the adult sex ratio was biased toward males, and in another six populations the adult sex ratio was biased toward females, the latter corresponding to the average adult sex ratio encountered in natural populations. In males the frequency and the degree of polygyny were lower in male-biased populations, as expected if competition among males determines polygyny. In females the frequency of polyandry was not different between treatments, and polyandrous females produced larger clutches, suggesting that polyandry might be adaptive. However, in male-biased populations females suffered from reduced reproductive success compared to female-biased populations, and the number of mate partners increased with female body size in polyandrous females. Polyandrous females of male-biased populations showed disproportionately more mating scars, indicating that polyandrous females of male-biased populations had more interactions with males and suggesting that the degree of multiple paternity is controlled by male sexual harassment. Our results thus imply that polyandry may be hierarchically controlled, with females controlling when to mate with multiple partners and male sexual harassment being a proximate determinant of the degree of multiple paternity. The results are also consistent with a sexual conflict in which male behaviors are harmful to females.     

Adaptation to monogamy influences parental care but not mating behavior in the burying beetle,Nicrophorus vespilloides

The mating system is expected to have an important influence on the evolution of mating and parenting behaviors. Although many studies have used experimental evolution to examine how mating behaviors evolve under different mating systems, this approach has seldom been used to study the evolution of parental care. We used experimental evolution to test whether adaptation to different mating systems involves changes in mating and parenting behaviors in populations of the burying beetle, Nicrophorus vespilloides. We maintained populations under monogamy or promiscuity for six generations. This manipulation had an immediate impact on reproductive performance and adult survival. Compared to monogamy, promiscuity reduced brood size and adult (particularly male) survival during breeding. After six generations of experimental evolution, there was no divergence between monogamous and promiscuous populations in mating behaviors. Parents from the promiscuous populations (especially males) displayed less care than parents from the monogamous populations. Our results are consistent with the hypothesis that male care will increase with the certainty of paternity. However, it appears that this change is not associated with a concurrent change in mating behaviors.     

The influence of maternal effects on indirect benefits associated with polyandry

Despite numerous and diverse theoretical models for the indirect benefits of polyandry, empirical support is mixed. One reason for the difficulty in detecting indirect benefits of polyandry may be that these are subtle and are mediated by environmental effects, such as maternal effects. Maternal effects may be especially important if females allocate resources to their offspring depending on the characteristics of their mating partners. We test this hypothesis in the burying beetle Nicrophorus vespilloides, a species that provides extensive and direct parental care to offspring. We used a fully factorial design and mated females to one, two, three, four or five different males and manipulated conditions so that their offspring received reduced (12 h) or full (ca 72 h) maternal care. We found that average offspring fitness increased with full maternal care but there was no significant effect of polyandry or the interaction between the duration of maternal care and the level of polyandry on offspring fitness. Thus, although polyandry could provide a mechanism for biasing paternity towards high quality or compatible males, and variation in parental care matters, we found no evidence that female N. vespilloides gain indirect benefits by using parental care to bias the allocation of resources under different mating conditions.     

Correlated evolution in parental care in females but not males in response to selection on paternity assurance behaviour

According to classical parental care theory males are expected to provide less parental care when offspring in a brood are less likely to be their own, but empirical evidence in support of this relationship is equivocal. Recent work predicts that social interactions between the sexes can modify co‐evolution between traits involved in mating and parental care as a result of costs associated with these social interactions (i.e. sexual conflict). In burying beetles (Nicrophorus vespilloides), we use artificial selection on a paternity assurance trait, and crosses within and between selection lines, to show that selection acting on females, not males, can drive the co‐evolution of paternity assurance traits and parental care. Males do not care more in response to selection on mating rate. Instead, patterns of parental care change as an indirect response to costs of mating for females.     

Devoted fathers or selfish lovers? Conflict between mating effort and parental care in a harem‐defending arachnid

When there is a temporal trade‐off between mating effort and parental care, theoretical models predict that intense sexual selection on males leads to reduced paternal care. Thus, high‐quality males should invest more in mating effort because they have higher chances of acquiring mates, whereas low‐quality males should bias their investment towards parental care. Once paternal care has evolved, offspring value should also influence males’ decisions to invest in offspring attendance. Here, we performed a manipulation under field conditions to investigate the factors that influence male allocation in either mating effort or parental care. We predicted that facultative paternal care in the harem‐holding harvestman Serracutisoma proximum would be negatively influenced by male attractiveness and positively influenced by offspring value. We found that attractive males were less likely to engage in egg attendance and that the higher the perceived paternity, the higher the caring frequency. Finally, egg mortality was not related to caring frequency by males, but predation pressure was much lower than that recorded in previous studies with the same population. Thus, the benefits of facultative male care may be conditional to temporal variation in the intensity of egg predation. In conclusion, males adjust their investment in either territory defence or egg attendance according to their recent mating history and perceived paternity. Our findings suggest that exclusive paternal care can evolve from facultative paternal care only if the trade‐off between mating effort and parental care is circumvented.