Variable Social Mating System in the Sedge Warbler,Acrocephalus schoenobaenus

We studied the mating system in a local population of colour-ringed sedge warblers in south Central Sweden in 1990–92. Of 58 territorial males, 59% were socially monogamous, 14% socially polygynous and 27% unpaired. Socially polygynous males in general paired with two females: the only exception was one male that formed pair bonds with three females. Among the males that formed a pair bond, 38% resumed singing after their first female had started egg-laying or incubation and 50% of the paired males that resumed singing succeeded in attracting a second female. Hence, despite a consistently male-biased sex ratio in the population a large proportion of the males tried to become polygynous and they were often successful. The frequency of extra-pair matings did not differ between monogamous and polygynous males. Of 47 breeding females, 6.4% were sequentially socially polyandrous. In two out of three cases, the females fed the young of their first broods until independence before initiating the second brood. In the third case the female deserted her newly fledged young and these were instead cared for by a neighbouring male. DNA fingerprinting revealed that this male had not sired any of these young. Each of the sequentially polyandrous females successfully raised both their broods, and their annual reproductive success was slightly higher than the average for the polygynous males. When the sequentially socially polyandrous females initiated their second brood, their primary male (in all cases polygynous males), cared for young in their secondary female's nest. In all cases, the sequentially polyandrous females formed second pair bonds with unpaired males that were close neighbors. This suggests that females switched pair male for their second brood to obtain a mate that was more likely to provide them with direct benefits (e.g. parental care).     

Coevolution of female fidelity and male help in populations with alternative reproductive tactics

In socially monogamous species, pair-bonded males often continue to provide care to all offspring in their nests despite some degree of paternity loss due to female extra-pair copulation. Previous theoretical models suggested that females can use their within-pair offspring as ‘hostages'' to blackmail their social mates, so that they continue to provide care to the brood at low levels of cuckoldry. These models, however, rely on the assumption of sufficiently accurate male detection of cuckoldry and the reduction of parental effort in case of suspicion. Therefore, they cannot explain the abundant cases where cuckolded males continue to provide extensive care to the brood. Here we use an analytical population genetics model and an individual-based simulation model to explore the coevolution of female fidelity and male help in populations with two genetically determined alternative reproductive tactics (ARTs): sneakers that achieve paternity solely via extra-pair copulations and bourgeois that form a mating pair and spend some efforts in brood care. We show that when the efficiency of mate guarding is intermediate, the bourgeois males can evolve to ‘specialize'' in providing care by spending more than 90% of time in helping their females while guarding them as much as possible, despite frequent cuckoldry by the sneakers. We also show that when sneakers have tactic-specific adaptations and thus are more competitive than the bourgeois in gaining extra-pair fertilizations, the frequency of sneakers and the degrees of female fidelity and male help can fluctuate in evolutionary cycles. Our theoretical predictions highlight the need for further empirical tests in species with ARTs.     

Parental behaviour in the Lapwing Vanellus vanellus

Parental behaviour of monogamous and polygynous Lapwings was studied during incubation and brood care. Both parents attended the nest in 86% of monogamous pairs ( n = 29 pairs). In 14% of pairs, only the male parent continued incubation until the eggs hatched, whereas the female deserted the clutch before or at the end of incubation. There was a clear division of parental roles during incubation. Females spent more time incubating (64% of time) than their mates (27%), whereas males spent more time defending the nest (3%) than females (>1%). Time spent incubating did not differ between monogamous and polygynous males. However, polygynous females spent more time incubating (primary females: 95%; secondary females: 97%) than monogamous females. Biparental care was the most common pattern of post-hatching care, although in some broods either the male or the female parent deserted before the chicks fledged. Division of sex roles was less pronounced in brood care than during incubation. Females spent more time brooding (21%) than males (3%), and females attended their chicks more closely than males. Nevertheless, males and females spent similar amounts of time defending the brood from predators and conspecifics. We suggest that the apparent division of parental roles may be explained by sexual selection, i.e. the remating opportunities for male Lapwings might be reduced if they increase their share in incubation. However, the different efficiency of care provision, for example in ability to defend offspring, may also influence the roles of the sexes in parental care.     

Parental Investment and Division of Labor in the Midas Cichlid (Cichlasoma citrinellum)

The Midas cichlid (Cichlasoma citrinellum) is an aggressive, monogamous fish living in the Great Lakes of Nicaragua. Its breeding success rates are low due to intense competition for breeding sites and high levels of predation on the young. Male Midas cichlids devote a small portion of body weight to gonads and gametes compared with females. Males produce relatively small amounts of sperm perhaps because cichlid fertilization is very efficient and the male has a high certainty of paternity. While pair members invest equal amounts of time in parental care over the course of the breeding cycle, there is a clear division of labor. Males invest more in territorial protection than do females, whereas females provide more nurturance. Both parents are active over the course of the cycle but the male invests more intensely in the early stages of the cycle. About the time the eggs hatch, the burden of care shifts to the female and she continues to invest significantly more than the male over the remainder of the cycle. Females invest much more than do males when tissue investment and parental behavior are combined. Females also assume more of the burden of care as the brood matures. The male is not free to take advantage of this and leave his mate to initiate other broods because two parents are needed to defend the breeding site and brood. Monogamy with biparental care results.     

Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird

Although many species form socially monogamous pair bonds, relevant neural mechanisms have been described for only a single species, the prairie vole (Microtus ochrogaster). In this species, pair bonding is strongly dependent upon the nonapeptides oxytocin (OT) and vasopressin, in females and males, respectively. Because monogamy has evolved many times in multiple lineages, data from additional species are required to determine whether similar peptide mechanisms modulate bonding when monogamy evolves independently. Here we test the hypothesis that OT-like receptor activation is required for pair bond formation in the socially monogamous zebra finch (Taeniopygia guttata). Males and females were administered chronic intracerebroventricular infusions of saline or an OT receptor antagonist and were observed twice daily for 3 days in a colony environment. A variety of affiliative, aggressive and other behaviours were quantified. The antagonist produced significant and selective effects on pair bonding (latency to pair; number of sessions paired; stable pairing) and the associated behaviour of allopreening. Importantly, findings for males follow the trends of females; this yields main effects of treatment in two-way ANOVAs, although within-sex analyses are significant only for females. These data provide evidence for both convergent evolution and species diversity in the neuroendocrine mechanisms of pair bonding.     

Physiological benefits of being small in a changing world: responses of Coho salmon (Oncorhynchus kisutch) to an acute thermal challenge and a simulated capture event

Evidence is building to suggest that both chronic and acute warm temperature exposure, as well as other anthropogenic perturbations, may select for small adult fish within a species. To shed light on this phenomenon, we investigated physiological and anatomical attributes associated with size-specific responses to an acute thermal challenge and a fisheries capture simulation (exercise+air exposure) in maturing male coho salmon (Oncorhynchus kisutch). Full-size females were included for a sex-specific comparison. A size-specific response in haematology to an acute thermal challenge (from 7 to 20 °C at 3 °C h(-1)) was apparent only for plasma potassium, whereby full-size males exhibited a significant increase in comparison with smaller males ('jacks'). Full-size females exhibited an elevated blood stress response in comparison with full-size males. Metabolic recovery following exhaustive exercise at 7 °C was size-specific, with jacks regaining resting levels of metabolism at 9.3 ± 0.5 h post-exercise in comparison with 12.3 ± 0.4 h for full-size fish of both sexes. Excess post-exercise oxygen consumption scaled with body mass in male fish with an exponent of b = 1.20 ± 0.08. Jacks appeared to regain osmoregulatory homeostasis faster than full-size males, and they had higher ventilation rates at 1 h post-exercise. Peak metabolic rate during post-exercise recovery scaled with body mass with an exponent of b~1, suggesting that the slower metabolic recovery in large fish was not due to limitations in diffusive or convective oxygen transport, but that large fish simply accumulated a greater 'oxygen debt' that took longer to pay back at the size-independent peak metabolic rate of ~6 mg min(-1) kg(-1). Post-exercise recovery of plasma testosterone was faster in jacks compared with full-size males, suggesting less impairment of the maturation trajectory of smaller fish. Supporting previous studies, these findings suggest that environmental change and non-lethal fisheries interactions have the potential to select for small individuals within fish populations over time.     

Sperm Competition in a Viviparous Fish

We investigated multiple paternity and sperm precedence in the Amarillo fish, Girardinichthys multiradiatus (Goodeidae). We allowed females to mate with two different-sized males consecutively and assessed the paternity of the ensuing broods using allozyme electrophoresis. We presented one-half of the females the larger, and the other half the smaller, male first. Allozyme variation among individuals was low, yielding conservative estimates of multiple paternity. Half the broods were of mixed paternity, but one male always sired more than 70% of the embryos in each brood. The proportion of the brood sired was not related to mating sequence, but when we classified males by relative size, the larger male of each pair usually fathered greater proportions of offspring than the smaller male. This association disappeared when we used the actual size of the males in the analysis. Instead, for any pair of males, the difference in number of offspring sired was correlated to differences in the rate of courtship displays, rather than size differences, suggesting that courtship intensity is a better predictor of paternity than male size. Within a pair, the larger male usually displayed more than the smaller one, but there was no correlation between male size and display rate across all males. Parsimony suggests a correlation between courtship rate and sperm production, but we cannot rule out the possibility that females allocate paternity according to the relative merits of the males.     

Polygyny in the tree swallow Tachycineta bicolor: a result of the cost of searching for an unmated male

The costs imposed by parental care duties on an individual's future survival and reproduction generate conflicts because parents should attempt to minimize their investment in the present brood, and exploit the parental care of the other parent. This conflict is likely to contribute to cases of both polygamy and desertion. Here, we study the costs of polygyny in the tree swallow Tachycineta bicolor , using observations on 52 nests that were attended by polygynous males over 14 y. Both females mated to polygynous males paid reproductive costs at several stages of the nesting cycle. Clutches laid by social mates of polygynous versus monogamous males did not differ in size. However, initial brood sizes for polygynously mated females were lower because a higher proportion of their eggs failed to hatch. Likewise, fledging success was lower and nest predation rates were higher, perhaps reflecting the direct or indirect effects of reduced male attention. These results demonstrate that females pay a productivity cost when breeding with reduced male parental care. In contrast, polygynous males fledge on average more young than monogamous ones and clearly benefit from the association. We suggest that a mate-search cost is leading to the few cases of polygamous males: although females are likely evaluating males for their prospective dedication to the breeding attempt, in a short-lived bird with a short breeding season, the cost to females of searching for a more dedicated male is the risk of not breeding at all.     

Should I stay or should I go? Female brood desertion and male counterstrategy in rock sparrows

Brood desertion involves a series of interactions between themembers of a pair. This process is likely to be based on eithermember's perception of the other's propensity to desert. Wemanipulated this perception in males by experimentally increasingfemale body mass in the rock sparrow (Petronia petronia), aspecies in which females can desert their first brood beforethe nestlings from the first brood leave the nest. We predictedthat the male would either desert the brood first or stay evenif this implied the risk of caring for the brood alone. We foundthat males mated to loaded females did not leave but stayedand significantly increased their courtship rate and mate guarding.Unexpectedly, they also increased their food provisioning tothe nestlings, even though loaded females did not reduce theirnestling-feeding rate. The increase in male feeding rate maybe explained as a way for the male to reduce the female's propensityto switch mate and desert or to increase her propensity to copulatewith the male to obtain paternity in her next brood. Altogether,our results demonstrate that the perception of the risk of beingdeserted by the female does not necessarily induce males todesert first, contrary to what is generally assumed by theoreticalmodels.     

Monogamous pair bonds and mate switching in the Western Australian seahorse Hippocampus subelongatus

Apparently monogamous animals often prove, upon genetic inspection, to mate polygamously. Seahorse males provide care in a brood pouch. An earlier genetic study of the Western Australian seahorse demonstrated that males mate with only one female for each particular brood. Here we investigate whether males remain monogamous in sequential pregnancies during a breeding season. In a natural population we tagged males and sampled young from two successive broods of 14 males. Microsatellite analyses of parentage revealed that eight males re‐mated with the same female, and six with a new female. Thus, in this first study to document long‐term genetic monogamy in a seahorse, we show that switches of mates still occur. Polygynous males moved greater distances between broods, and tended to have longer interbrood intervals, than monogamous males, suggesting substantial costs associated with the breaking of pair bonds which may explain the high degree of social monogamy in this fish genus.     

Pigment-based skin colour in the blue-footed booby: an honest signal of current condition used by females to adjust reproductive investment

In monogamous species, the value of present reproduction is affected by the current condition of the mate, and females may use male ornaments to evaluate his condition and adjust their level of investment according. Many animals display colour in fleshy structures which may be accurate indicators of quality due to their potentially rapid response to changes in condition. Here we show that in the blue-footed booby, Sula nebouxii, male foot colour is structurally (collagen arrays) and pigment based. In 48 h foot colour became duller when males were food deprived and brighter when they were re-fed with fresh fish. Variation of dietary carotenoids induced comparable changes in cell-mediated immune function and foot colour, suggesting that carotenoid-pigmentation reveals the immunological state of individuals. These results suggest that pigment-based foot colour is a rapid honest signal of current condition. In a second experiment, we found that rapid variation in male foot colour caused parallel variation in female reproductive investment. One day after the first egg was laid we captured the males and modified the foot colour of experimental males with a non-toxic and water resistant duller blue intensive make-up, mimicking males in low condition. Females decreased the size of their second eggs, relative to the second egg of control females, when the feet of their mates were experimentally duller. Since brood reduction in this species is related to size differences between brood mates at hatching, by laying lighter second eggs females are facilitating brood reduction. Our data indicate that blue-footed booby females are continuously evaluating their mates and can perform rapid adjustments of reproductive investment by using dynamic sexual traits. We suggest that this fine-tuned adjustment may be widespread in socially monogamous animals.     

Monogamy and sex role reversal in the pipefish Corythoichthys haematopterus

We observed the mating pattern and social behaviour of the pipefish Corythoichthys haematopterus in temperate waters of Japan during three successive breeding seasons. Males cared for a clutch in their brood pouch for 9-19 days until hatching and had several broods in the season with nonbrooding intervals of only 1 or 2 days. The population sex ratio was female biased and some females were always excluded from reproduction. Although males were sometimes courted by unmated females together with their regular partners, they always mated with the latter. The pair bond was maintained until the next season if both members survived. When males lost their partners, they remated with neighbouring unmated females within a few days. In contrast, widowed females remained unmated for a long time. Females had larger home ranges and were more active in courtship displays than males. This pipefish provides the first example of sex role reversal among monogamous syngnathid fish. We suggest that mate guarding by females is a primary proximate factor for maintenance of monogamy in this fish. Copyright 2001 The Association for the Study of Animal Behaviour.     

Carrier females and sender males: An evolutionary hypothesis linking female attractiveness,family resemblance,and paternity confidence

The article introduces and elaborates the hypothesis of carrier features, characteristics which in females are attractive to males as mate-choice cues. Female carrier features increase paternal resemblance and are ultimately attractive because they help pair-bonded males distinguish genetic offspring from those conceived by mates in extra-pair copulations. The proposed kin recognition mechanism, whether culturally evolved or innate, facilitates discriminatory paternal investment, and hence male fitness. Carrier features would be attractive to males in monogamous species where paternal investment is high, and cuckoldry represents a significant risk to male fitness. Logical space exists for male sender features, which tend to be expressed in offspring regardless of female characteristics. Conflict of genetic interests between the sexes should favor the evolution of carrier, rather than sender, features in both sexes. The argument centers on humans, for whom candidate carrier features are discussed with regard to physiognomy, behavior, recessive traits, and body odor. Criticisms are discussed, and testable predictions enumerated.     

No evidence for increased offspring heterozygosity from extrapair mating in the reed bunting (Emberiza schoeniclus)

It has been hypothesized that females mate multiply to increasethe heterozygosity of their progeny because heterozygous individualsare assumed to have a fitness advantage. Females can maximizeheterozygosity of their offspring by mating with geneticallyunrelated and/or heterozygous males. We tested these predictionsin a socially monogamous passerine, the reed bunting (Emberizaschoeniclus), where extrapair paternity occurs frequently. Theresults based on genotypes at nine microsatellite loci revealedthat females were no less genetically related to the extrapairmale(s) (EPMs) than to their pair male (i.e., breeding partner)and that EPMs were no more heterozygous than the males theycuckolded. In addition, a direct comparison of maternal half-siblingsnaturally raised in the same brood showed that extrapair youngwere no more heterozygous than within-pair young. Thus, femalereed buntings do not seem to mate with EPMs to increase offspringheterozygosity. It is not yet known whether extrapair matinginvolves any benefits at all to females in this species.     

Pair bond duration influences paternal provisioning and the primary sex ratio of brown thornbill broods

Parents should vary their level of investment in sons and daughters in response to the fitness costs and benefits accrued through male and female offspring. I investigated brood sex ratio biases and parental provisioning behaviour in the brown thornbill, Acanthiza pusilla, a sexually dimorphic Australian passserine. Parents delivered more food to male-biased than female-biased broods. However, factors determining parental provisioning rates differed between the sexes. Female provisioning rates were related to brood sex ratio in both natural and experimental broods with manipulated sex ratios. In contrast, male provisioning rates were not affected by brood sex ratio in either natural or experimental broods. However, males in established pairs provisioned at a higher rate than males in new pairs. Data on the sex ratio of 109 broods suggest that female brown thornbills adjust their primary sex ratio in response to pair bond duration. Females in new pairs produced broods with significantly fewer sons than females in established pairs. This pattern would be beneficial to females if the costs of rearing sons were higher for females in new than established pairs. This may be the case since females in new pairs provisioned experimental all-male broods at elevated rates. The condition of nestlings also tended to decline more in these all-male broods than in other experimental broods. This will have additional fitness consequences because nestling mass influences recruitment in thornbills. Female thornbills may therefore obtain significant fitness benefits from adjusting their brood sex ratio in response to the status of their pair bond. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Correlates of complete brood failure in blue tits: could extra‐pair mating provide unexplored benefits to females?

Behavioural ecologists have for decades investigated the adaptive value of extra‐pair copulation (EPC) for females of socially monogamous species. Despite extensive effort testing for genetic benefits, there now seems to be a consensus that the so‐called ‘good genes’ effects are at most weak. In parallel the search for direct benefits has mostly focused on the period surrounding egg laying, thus neglecting potential correlates of EPC that might be expressed at later stages in the breeding cycle. Here we used Bayesian methods to analyse data collected over four years in a population of blue tits Cyanistes caeruleus, where no support was previously found for ‘good genes’ effects. We found that broods with mixed paternity experienced less brood failure at the nestling stage than broods with single paternity, and that females having experienced complete brood failure in their previous breeding attempt had higher rates of mixed paternity than either yearling or previously successful females. To better understand these observations we also explored relationships between extra‐pair mating, male and female phenotype, and local breeding density. We found that in almost all cases the sires of extra‐pair offspring were close neighbours, and that within those close neighbourhoods extra‐pair sires were older than other males not siring extra‐pair offspring. Also, females did not display consistent EPC status across years. Taken together our results suggest that multiple mating might be a flexible female behaviour influenced by previous breeding experience, and motivate further experimental tests of causal links between extra‐pair copulation and predation.     

Mate size and breeding success in a monogamous cichlid fish

Synopsis The patterns of mate size and parental care of a monogamous cichlid fish,Cichlasoma maculicauda, were studied in Gatun Lake, Panama. Males defend territories which serve as courtship and nest sites. Within a population most mates in pairs are of equal size rank. In each pair the male is larger than the female, probably because most mature males are larger than most mature females. Clutch size increases with female body size. Male size affects breeding success in two ways. First, larger males provide nest sites less susceptible to destructive wave action. Second, young of larger males grow faster than young of smaller males. Large males defeat small males in contests for position in feeding areas, and this may provide their young with better feeding conditions. In the laboratory young growth rates increase with food abundance, and at high levels of food surpass those observed in nature. Fast growth of young reduces their vulnerability to predators and should allow parents to breed more often. Young survival rates improve with the size of the parents, so that larger fish raise more offspring at each breeding attempt. These observations suggest why preference for large mates should occur.     

The effects of neonatal paternal deprivation on pair bonding, NAcc dopamine receptor mRNA expression and serum corticosterone in mandarin voles

High levels of paternal care are important for the development of social behavior in monogamous rodents. However, the effects of paternal care on the formation of pair bonding and underlying neuroendocrine mechanisms, especially the involvements of dopamine system and corticosterone, are not well understood. We investigated effects of paternal deprivation on pair bonding in mandarin voles (Microtus mandarinus), a socially monogamous rodent. Paternal deprivation was found to inhibit the formation of pair bonding in females according to partner preference tests (PPT). Paternal deprivation also reduced body contact behavior and increased aggression in males and females in PPT. During social interaction tests (SIT), paternal deprivation was found to reduce investigative and aggressive behaviors but increase body contact and self-grooming in females, and reduce staring, aggression, body contact and self-grooming in males when interacting with the opposite sex. Paternal deprivation reduced the expression of dopamine 1-type receptor (D1R) mRNA and dopamine 2-type receptor (D2R) mRNA in the nucleus accumbens of female offspring in later life, but enhanced mRNA expression of these two dopamine receptors in males. After three days of cohabitation the expression of D1R mRNA and D2R mRNA was negatively correlated for voles reared by two parents, but positively correlated in paternally deprived animals. Paternal deprivation reduced serum corticosterone levels in females but had the opposite effect in males. Three days of cohabitation did not alter corticosterone levels of PD females, but reduced it in PC females. Our results provide substantial evidence that paternal deprivation inhibits the formation of pair bonding in female mandarin voles and alters social behavior later in life. These behavioral variations were possibly associated with sex-specific alterations in the expression of two types of dopamine receptors and serum corticosterone levels induced by paternal deprivation.     

Paternal influence on growth and survival of dark-eyed junco young: do parental males benefit?

Recent studies of typically monogamous passerine birds have suggested that the fitness benefits males derive by caring for their young may not be as great as was previously thought. This study was conducted to determine whether parental care by male dark-eyed juncos, Junco hyemalis, serves to increase either the quantity or quality of young that they produce. Over a 4-year period, males were caught at the time their eggs hatched, and the subsequent growth and survival of the young of unaided females and control pairs were compared. Broods raised by unaided females gained body mass more slowly and fledged at slightly lower mass than those raised by two parents. However, fledging mass was not correlated with survival to independence. There were no differences in tarsus growth between the two treatment groups. Entire brood loss to predators occurred as often among females without male help as it did among those with male help. However, partial brood loss was more common among female-only broods than among controls; this difference was largely attributable to higher rates of starvation and exposure in female-only broods. There appeared to be an interaction between growth and predation. Female-only broods that were below the median mass of combined treatment groups at 5 days of age were more likely than all other broods to experience partial or complete predation. Male impact on offspring survival varied with age of the offspring. When years were combined, males tended to increase survival during the first half of the nestling period, but their impact at the time of nest-leaving was minimal. In all years, from nest-leaving to independence (ca. 2 weeks), broods without male help survived only about half as well as did those with male help. Independent young raised by one parent were as likely to return the following spring as were young raised by two parents. Thus, paternal care benefits males by improving the survivorship of their fledglings, and may also act as a buffer against poor female parental quality and inclement weather. However, the magnitude of these benefits is such that bigamous males might achieve greater reproductive success than monogamous males. Various possible male strategies are discussed.     

Sexual conflict and parental care in magnificent frigatebirds: full compensation by deserted females

Parental care is a cooperative venture between a male and a female in many socially monogamous birds. Care is costly, and thus, sexual conflict arises between the parents about how much effort they should invest into rearing their young. The sexual conflict over care is most apparent when one parent abandons the brood before the offspring are independent. The deserted parent has three options: (1) desert the brood because a single parent is unable to raise the young on its own; (2) continue care provision at the same level as during biparental care, and thus do not compensate for the absence of mate; or (3) increase care and compensate partially or totally. We investigated these options in the magnificent frigatebird, Fregata magnificens, a species in which the male deserts his mate and brood before the chick is independent. During biparental care, females fed the chick more often than the males. After their mate deserted, the females nearly doubled their feeding rate and thus, fully compensated for the lost care. Consistent with these observations, growth rates of chicks provided with biparental and female-only care did not differ. These results support recent theoretical models of parental care, and suggest that females may withhold care during biparental care to manoeuvre their mates into prolonged care provision. A female only provides at her full capacity once her mate has deserted.