Socially induced delayed primiparity in brown bears Ursus arctos

Reproductive suppression through behavioral or physiological means is common in group-living and cooperative breeding mammals, but to our knowledge it has not been shown in wild large carnivores other than those with a clear form of social organization. Brown bear (Ursus arctos) females form matrilinear assemblages with related females using a common and largely exclusive area. Behavioral reproductive suppression might develop due to a hierarchical system among females within a matrilinear assemblage or due to inbreeding avoidance, because male brown bears can overlap with their daughters. We tested whether natal dispersal influenced the age of primiparity. We predicted that emigrant females, geographically removed from maternal or paternal influence, would reproduce earlier than philopatric females. The average age of primiparity was 4.3 years in females that dispersed outside their mother’s home range (n=8) and 5.2 years in philopatric females (n=10). Only the overlap with the mother’s home range, and not body size, body mass, growth, local population density, or overlap with the father’s home range, had a significant influence on the age of primiparity. The ultimate role of reproductive suppression for brown bears is likely to avoid inbreeding or to minimize resource competition. Due to the low risk of inbreeding and frequent exposure of young females to unrelated males, we conclude that resource competition within female hierarchies causes reproductive suppression in young females.     

Costs of delayed dispersal and alloparental care in the fungus-cultivating ambrosia beetle <Emphasis Type="Italic">Xyleborus affinis</Emphasis> Eichhoff (Scolytinae: Curculionidae)

Body reserves may determine the reproductive output of animals, depending on their resource allocation strategy. In insects, an accumulation of reserves for reproduction is often obtained before dispersal by pre-emergence (or maturation) feeding. This has been assumed to be an important cause of delayed dispersal from the natal nest in scolytine beetles. In the cooperatively breeding ambrosia beetles, this is of special interest because in this group delayed dispersal could serve two alternative purposes: “selfish” maturation feeding or “altruistic” alloparental care. To distinguish between these two possibilities, we have experimentally studied the effect of delayed dispersal on future reproductive output in the xyleborine ambrosia beetle Xyleborus affinis. Females experimentally induced to disperse and delayed dispersing females did not differ in their body condition at dispersal and in their founding success afterwards, which indicates that females disperse independently of condition, and staying adult females are fully mature and would be able to breed. However, induced dispersers produced more offspring than delayed dispersers within a test period of 40 days. This suggests that delayed dispersal comes at a cost to females, which may result primarily from alloparental care and leads to a reduced reproductive output. Alternatively, females might have reproduced prior to dispersal. This is unlikely, however, for the majority of dispersing females because of the small numbers of offspring present in the gallery when females dispersed, suggesting that mainly the foundress had reproduced. In addition, “gallery of origin” was a strong predictor of the reproductive success of females, which may reflect variation in the microbial complex transmitted vertically from the natal nest to the daughter colony, or variation of genetic quality. These results have important implications for the understanding of proximate mechanisms selecting for philopatry and alloparental care in highly social ambrosia beetles and other cooperatively breeding arthropods.     

Sequential polyandry by brood desertion increases female fitness in a bird with obligatory bi-parental care

Parental care may be costly to parents because it decreases resources allocated to self-maintenance and may thus reduce survival and future reproductive success. An inter-sexual conflict may exist in animals with obligatory bi-parental care, such as birds of prey, in which females incubate and brood, whereas males provision food for their families. We analysed 29 years of data (1981–2009) from a study population of Tengmalm’s owls Aegolius funereus in western Finland to examine the occurrence and timing of brood desertion and sequential polyandry, and recorded a total of 1,123 monogamous and 12 polyandrous females. These data were supplemented with the 29-year nationwide Finnish ringing data, which included 11,590 monogamous and 20 polyandrous females. The 12 polyandrous females started egg-laying in their two nests at intervals of 54–68 days (mean 60 days), thus deserting their first broods when the age of oldest young averaged 21 days. Thirty-two polyandrous females re-mated and raised a second brood at a median distance of 4.5 km (range 1–196 km). These females produced 79% more eggs, 93% more hatchlings and 73% more fledglings than did females that laid simultaneously but remained monogamous. Our results show that not only males, but also females of altricial species with bi-parental care can increase their fitness by deserting their first brood when it will be cared for by the males. Earlier studies have shown that male owls can increase their lifetime reproductive success by simultaneous polygyny, and we suggest that an inter-sexual “tug-of-war” over bi-parental care exists in Tengmalm’s owls.     

Common goldeneyes adjust maternal effort in relation to prior brood success and not current brood size

Parental investment theory predicts that parental effort should be related to the reproductive value of the current brood. This depends on both the number of young and the survival prospects of each of them. Thus parents may provide more care to larger broods either because of (1) the direct effect of brood size per se on reproductive value (the “brood size” hypothesis) or because (2) past mortality, reflected in current brood size, predicts future mortality of the brood and hence its reproductive value (the “brood success” hypothesis). Earlier studies have not attempted to distinguish between these alternatives. We tested the hypotheses in the precocial, nidifugous common goldeneye Bucephala clangula, a species with uniparental female care. Maternal effort was measured as the time spent by the female in rearing the brood. We found that brood size itself is not associated with maternal effort, but that females modify their maternal effort according to the mortality already experienced by the brood, supporting the prediction of the brood success hypothesis. We also found that brood mortality varied considerably between broods and that previous mortality predicts future mortality within broods, basic assumptions of the brood success hypothesis. Received: 30 January 1996 / Accepted after revision: 27 October 1996     

Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons

Maternal investment in offspring is expected to vary according to offspring sex when the reproductive success of the progeny is a function of differential levels of parental expenditure. We conducted a longitudinal investigation of rhesus macaques to determine whether variation in male progeny production, measured with both DNA fingerprinting and short tandem repeat marker typing, could be traced back to patterns of maternal investment. Males weigh significantly more than females at birth, despite an absence of sex differences in gestation length. Size dimorphism increases during infancy, with maternal rank associated with son’s, but not daughter’s, weight at the end of the period of maternal investment. Son’s, but not daughter’s, weight at 1 year of age is significantly correlated with adult weight, and male, but not female, weight accounts for a portion of the variance in reproductive success. Variance in annual offspring output was three- to fourfold higher in males than in females. We suggest that energetic costs of rearing sons could be buffered by fetal delivery of testosterone to the mother, which is aromatized to estrogen and fosters fat accumulation during gestation. We conclude that maternal investment is only slightly greater in sons than in daughters, with mothers endowing sons with extra resources because son, but not daughter, mass has ramifications for offspring sirehood. However, male reproductive tactics supersede maternal investment patterns as fundamental regulators of male fitness. Received: 23 July 1999 / Received in revised form: 23 February 2000 / Accepted: 13 March 2000     

Reproductive success in a low skew, communal breeding mammal: the banded mongoose, Mungos mungo

In most cooperatively breeding species, reproduction is monopolised by a subset of group members. However, in some species most or all individuals breed. The factors that affect reproductive success in such species are vital to understanding why multiple females breed. A key issue is whether or not the presence of other breeders is costly to an individual’s reproductive success. This study examines the factors that affect the post-parturition component of reproductive success in groups of communal-breeding banded mongoose (Mungos mungo), where up to ten females breed together. Per-litter reproductive success was low (only 18% of pups survived from birth to independence). Whilst singular breeding was wholly unsuccessful, there were costs associated with breeding in the presence of increasing numbers of other females and in large groups. Synchronisation of parturition increased litter success, probably because it minimises the opportunity for infanticide or decreases competitive asymmetry between pups born to different females. There was no evidence of inbreeding depression, and reproductive success was generally higher in litters where females only had access to related males within their group. I conclude that communal breeding in female banded mongooses represents a compromise between the benefits of group-living and communal pup care on the one hand, and competition between females to maximise their personal reproductive success on the other. Such conflicts are likely to occur in most communal breeding species. Whilst communal breeding systems are generally considered egalitarian, negative effects of co-breeders on individual reproductive success is still an issue.     

Benefits of large broods by higher chick survival and better territories in a precocial shorebird

When reproductive success is constant in one breeding phase, different tactics that increase variation in reproductive success among individuals may evolve in other phases. For instance, in shorebirds, which usually have a limited clutch size of four eggs, variation in reproductive tactics among individuals is expected either before egg-laying (e.g. diverse mating systems) or after hatching of the young (e.g. diverse parental care). In this paper, I studied the pied avocet (Recurvirostra avosetta), a shorebird with a modal clutch size of four eggs, to test whether post-hatch chick adoption as an alternative tactic can be linked to increased variation in annual reproductive success. When predation was high, naturally adopting pairs produced more filial fledglings than did pairs not adopting chicks and not losing chicks to adoption. The number of filial fledglings increased with the number of adopted young, possibly through diluting the chances of predation on filial young. Experimental chick addition did not lead to more fledged young due to low brood integrity as shown by the frequent loss of chicks from some experimental broods. When predation was low, larger broods occupied feeding territories with higher prey abundance than smaller broods, possibly due to their dominance over smaller ones. Pairs that lost chicks to adoption (donors) fledged as many filial young in their broods as did non-adopters/non-donors, whereas the total number of donors’ filial fledglings, including those raised in adopting broods, approached that of adopters. These findings show, for the first time, that post-hatch alternative reproductive tactics can lead to variation in annual reproductive success and to higher success for some pairs even in species where past adaptations limit variation in reproductive success in a certain phase of reproduction.     

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

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

Cooperative breeding increases reproductive success in the social spider <Emphasis Type="Italic">Stegodyphus dumicola</Emphasis> (Araneae,Eresidae)

Sociality in some birds, mammals, and social insects was suggested to have evolved through the lengthening and extension of parental care behaviors to nondirect descendents. In these systems, group members care for young cooperatively and, thus, increase the reproductive success of the breeders and fitness of the young. Parental care behaviors, such as regurgitation feeding and matriphagy (consumption of the mother), occur in several subsocial and social spiders. However, it is not known whether females in a colony cooperate in caring for the young of other females and whether such cooperative care improves reproductive success. To answer this question, we created experimental colonies of the social spider Stegodyphus dumicola (Araneae, Eresidae), allowing only one female in a group to produce young, simulating reproductive skew occurring in nests in nature. In this paper, we show for the first time that females of S. dumicola cooperate in providing regurgitated food for young of other females and are even eaten by those young. Young raised by a group of females were larger and had greater survival than young raised only by their mother. Thus, fitness benefits from raising broods cooperatively may have favored the evolution of sociality in spiders.     

Weight comparisons and litter size manipulation in Columbian ground squirrels (Spermophilus columbianus) show evidence of costs of reproduction

I studied reproductive costs in the female Columbian ground squirrel (Spermophilus columbianus) using individually marked animals. I compared weight changes during the active season and over winter, and mortality for females that did and did not wean young. Females raising young were heavier at emergence in that spring than unsuccessful ones. Females that did not raise young gained more weight during summer, were heavier than successful females at the time of entry into hibernation, and were heavier emerging from hibernation the following spring. Over-winter mortality was higher for females that reared young compared to reproductively unsuccessful females. A food supplementation experiment showed that energy-rich food can accelerate individuals’ weight gain. Interactions between litter size, birth weight, weight at emergence from the natal burrow, survival of young to yearling age, and maternal fitness were also studied. Litter sizes were experimentally manipulated to evaluate how females cope with costs of rearing one additional young. Birth weight of juveniles was positively correlated with survival to emergence from the natal burrow and with survival to yearling age. Partial litter loss was higher in experimentally enlarged litters than in either experimentally decreased or control litters. Total litter loss, survival of adult females or the probability of weaning young the following year were not affected by the litter size manipulation. Females appear to adjust the size of their litter before birth, and to some extent during lactation, to their ability to wean young. Received: 20 January 2000 / Received in revised form: 12 March 2000 / Accepted: 18 March 2000     

Asymmetric sexual conflict over parental care in a biparental cichlid

Theoretical models predict that parents should adjust the amount of care both to their own and their partner’s body condition. In most biparental species, parental duties are switched repeatedly allowing for repeated mutual adjustment of the amount of care. In the mouthbrooding cichlid Eretmodus cyanostictus, terms are switched only once with females taking the first share. The timing of the shift of the clutch between mates strongly determines both partners’ brooding period and thereby their parental investment. Females signal their readiness to transfer the young several days before the male finally takes them, suggesting sexual conflict over the timing of the shift. In a lab experiment, we reduced the body condition of either the female or the male of a pair to test whether energy reserves affect the timing of the shift and whether female signalling behaviour depends on energetic state. Males with a lowered condition took the young later and incubated for a shorter period, which prolonged the incubation time of their female partners. When female condition was lowered, female and male incubation durations remained unchanged, although females signalled their readiness to shift more intensely. Our results suggest that males adjust their parental investment to own energy reserves but are unresponsive to their mate’s condition. Females appear to carry the entire costs for the male’s adjustment of care. We propose that intrinsic asymmetries in the scope for mutual adjustment of parental investment and the costs of negotiation crucially influence solutions of the conflict between sexes over care.     

Dominance status influences female reproductive strategy in a territorial African rodent <Emphasis Type="Italic">Rhabdomys pumilio</Emphasis>

Dominance status influences the fitness of many mammals. Using African striped mice Rhabdomys pumilio, we tested whether (1) dominant females have greater reproductive success than subordinate females, (2) dominant females influence the reproductive output of subordinate females when they are housed in close proximity, (3) reproductive output of a female changes in response to the dominance status of her neighbours, and (4) whether prolonged association between individuals influences the variance in reproductive success between dominants and subordinates (i.e. the ‘dear enemy’ phenomenon). The size and mass of litters of dominants increased significantly when housed adjacent to subordinates than when housed apart. The litter size and mass of subordinates remained unchanged, although subordinates spent significantly more time with their pups when housed close to dominants than when housed apart; time spent with pups by dominants remained unchanged. Moreover, females modified their reproductive output and behaviour in relation to the dominance status of their neighbours. Following prolonged association, dominants still had greater reproductive success, but now, the time spent with pups decreased in subordinates. We suggest that dominants adopt a strategy to increase the reproductive value of their litter, whereas subordinates adopt a pup defence strategy. These strategies are flexible and are influenced by the dominance status and period of association between neighbours, so that females could maximize their fitness in response to varying social conditions.     

Asymmetric costs favor female desertion in the facultatively polyandrous northern flicker (Colaptes auratus): a removal experiment

Previous studies of biparental care in birds have focused on the males contribution and experimental removal of males. Woodpeckers, with a high level of paternal care including nocturnal incubation and brooding by males, offer a meaningful system in which to examine the importance of care by females. I studied the reproductive performance of 17 widowed male and 8 widowed female northern flickers (Colaptes auratus) relative to biparental (control) pairs. Of these single parents all widowed shortly after hatching, only one female abandoned its nest. Single parents boosted their provisioning rates to achieve 83% the provisioning rate of control broods, but reared significantly fewer young and young of poorer quality. However, single males, with 85% of the reproductive success of controls, were more successful than females with 43% the success of controls. Among widowed birds, a not significant lower survival was observed, but the chance of re-pairing with the same partner in a subsequent year was only 16% in the natural population, so long-term costs of desertion may be small. Although females seem to have the incentive and ability to desert, a lack of available males may constrain opportunities. This study demonstrates that when parental care roles are reversed in altricial birds, asymmetric benefits can favor female and not male desertion.     

Female reproductive strategies in bar-headed geese (Anser indicus): Why are geese monogamous?

Summary In a semi-captive flock of Anser indicus with a surplus of females, permanent harem groups consisting of one male with one to five females, lasting for up to several years, were regularly observed. Polygynous groups contain one paired female to which the male is most attentive and secondary females which follow the paired male and are tolerated by the pair. Average annual reproductive success was lowest in lone females (0.02 young fledged per year), higher in secondary females (0.23 young) and highest in paired females (0.56 young per year). Differences seemed due to different degrees of male assistance. Secondary females could not be shown to be competitors of paired females in annual reproductive success. Lone females became secondary females mainly after an age of 3 years, i.e. when their chances to pair had dropped significantly. Females were more likely to become secondary instead of paired females in years when the adult sex ratio was more heavily female biased. As sex ratios in wild geese are usually around 1:1 or even biased towards males, females will not usually need to resort to the suboptimal secondary-female strategy. Hence, geese usually live in monogamous pairs instead of harem groups.     

Prenatal social conditions shape offspring adult phenotype and reproductive success

The prenatal social environment affects offspring development in most studied taxa with potentially lifelong consequences. To understand the adaptive significance of such maternal influences on offspring development, it is important to study their effects on fitness. In guinea pigs, social instability during pregnancy leads to delayed development of male offspring. This has been interpreted as an adaptation to high social densities, where young males need to queue for reproductive opportunities since they cannot out-compete older dominant males. The consequences for male reproductive success are, however, so far unknown. To study the effects of different prenatal social densities on offspring reproductive performance, we housed females individually or in small groups during late pregnancy. Offspring from both treatments were reared together in large groups until independence and thereafter housed in same-sex pairs of the same treatment. We then observed courtship, aggressive behavior, and reproductive success in a low-density context with one male from each treatment competing over access to two females. Sons born to individually housed females initiated more fights, had more social contacts, courted females more, and had a higher reproductive success than sons of group-housed females. Sons born to mothers experiencing low social densities before birth therefore perform better at low social group sizes, suggesting that male development may be adaptively adjusted to anticipated social densities, although performance under high densities still needs to be compared.     

Multiple insemination increases reproductive success of female Montandon’s newt (<Emphasis Type="Italic">Triturus montandoni</Emphasis>, Caudata,Salamandridae)

The adaptive significance of multiple matings for females is a matter of much controversy. In insects, supplying the female’s sperm reserves with portions of fresh spermatozoa may be the main function of multiple matings. This simple explanation may also be applied to other animals which produce large numbers of eggs over prolonged periods of time. We tested the fertility insurance hypothesis in Montandon’s newt (Triturus montandoni, Amphibia, Salamandridae). T. montandoni females are inseminated internally by spermatophores they have picked up, and subsequently lay eggs fertilized by spermatozoa released from the spermatheca. We compared the reproductive success of singly and multiply inseminated females of Montandon’s newt in the laboratory. Multiply inseminated females laid more eggs and had a lower percentage of non-developing eggs than females who mated only once. Our data suggest that remating increases the reproductive success of multiply inseminated females by replenishing sperm reserves in the spermatheca or by supplying females with fresh portions of spermatozoa with high fertilizing capacity. Received: 7 January 2000 / Revised: 13 September 2000 / Accepted: 7 October 2000     

Mating system and individual reproductive success of sympatric anadromous and resident brook charr, <Emphasis Type="Italic">Salvelinus fontinalis</Emphasis>, under natural conditions

Salmonids are known for the occurrence in sympatry of two life-history forms, one that undergoes migration to sea before returning to freshwater to reproduce (anadromous) and one that inhabits freshwater without a migration phase (resident). Whereas one breeding population is often suggested by population genetic studies, mating patterns have rarely been directly assessed, especially when both sexes are found within each life-history form. By using highly polymorphic microsatellite loci and parentage analysis in a natural population of sympatric anadromous and resident brook charr (Salvelinus fontinalis), we found that gene flow occurred between the two forms and was mediated by resident males mating with both resident and anadromous females. Determinants of reproductive success, estimated by the number of surviving juveniles (ages 1 and 2 years), differed between the sexes. No strong evidence of the influence of size on individual reproductive success was found for males, whereas larger females (and hence most likely to be anadromous) were more successful. The higher individual reproductive success of anadromous fish compared to residents was mainly explained by this higher reproductive success of anadromous females. We suggest that resident males adopt a “sneaking” reproductive tactic as a way of increasing their reproductive success by mating with females of all sizes in all habitats. The persistence of the resident tactic among females may be linked to their advantage in accessing spatially constrained spawning areas in small tributary streams unavailable to larger females.     

Tug-of-war over reproduction in a cooperatively breeding cichlid

In group-living animals, dominants may suppress subordinate reproduction directly and indirectly, thereby skewing reproduction in their favour. In this study, we show experimentally that this ability (‘power’) is influenced by resource distribution and the body size difference between unrelated dominants and subordinates in the cichlid Neolamprologus pulcher. Reproduction was strongly skewed towards the dominant female, due to these females producing more and larger clutches and those clutches surviving egg eating better than those of subordinate females, but was not so when subordinates defended a patch. If breeding shelters were provided in two patches, subordinate females were more likely to exclusively defend a patch against the dominant female and breed, compared to when the same breeding resource was provided in one patch. Relatively large subordinate females were more likely to defend a patch and reproduce. Females also directly interfered with each other’s reproduction by eating the competitors’ eggs, at which dominants were more successful. Although dominant females benefited from subordinate females due to alloparental care and an increase in egg mass, they also showed costs due to reduced growth in the presence of subordinates. The results support the view that the dominant’s power to control subordinate reproduction determines reproductive partitioning, in agreement with the predictions from tug-of-war models of reproductive skew.     

Reproduction by subordinates in cooperatively breeding Arabian babblers is uncommon but predictable

In a genetic analysis of the mating system of cooperatively breeding Arabian babblers (Timalidae: Turdoides squamiceps), we identified which individuals in the population are breeding, and how reproductive success was distributed among group members with respect to their dominance rank, for both males and females. The population was characterized by an asymmetrical distribution of reproductive success; behaviorally dominant males produced 176 of 186 (95%) of the offspring in 44 social groups analyzed, and alpha females produced 185 of 186 (99.5%). We evaluated models of reproductive skew by examining genetic and demographic correlates of reproduction by␣subordinates. Subordinate (beta) males that sired young were more likely to be recent dispersers from their natal groups or members of newly formed groups than betas that did not reproduce. Breeding beta males had spent smaller proportions of their lives with the current alpha male and female as alphas than had beta males that did not sire young. One consequence of the linkage of dispersal with breeding in newly formed, nonnatal groups is that beta males that sired young had significantly lower genetic similarity to the alpha males in their groups (based on band-sharing coefficients using multilocus minisatellite DNA fingerprinting) than those that did not sire young. This pattern may occur generally in species in which group membership accrues both through nondispersal of young (forming groups of relatives) as well as through dispersal involving coalitions that sometimes include nonrelatives. Received: 22 July 1997 / Accepted after revision: 5 February 1998     

Mate choice games, context-dependent good genes, and genetic cycles in the side-blotched lizard, Uta stansburiana

According to mate choice models, a female should prefer males with traits that are reliable indicators of genetic quality which the sire can pass on to their progeny. However, good genes may depend on the social environment, and female choice for good genes should be context dependent. The side-blotched lizard, Uta stansburiana, exhibits genetically based throat colors (orange, blue, or yellow) that could be used as a sexually selected signal since they reliably predict the genetic quality of mates. The frequencies of male and female morphs cycle between years, and both male and female morphs have an advantage when rare; thus genetic quality will depend on morph frequency. A female should choose a sire that maximizes the reproductive success of both male and female progeny. We examine a game theoretical model that predicts female mate choice as a function of morph frequency and population density. The model predicts the following flexible mate choice rule: both female morphs should prefer rare males in ’boom years’ of the female cycle (e.g., ’rarest-of-N rule’), but prefer orange males in ’crash years’ of the female cycle (’orange-male rule’). Cues from the current social environment should be used by females to choose a mate that maximizes the future reproductive success of progeny, given the social environment of the next generation. We predict that the cue is the density of aggressive orange females. In the side-blotched lizard, cycling mate choice games and context-dependent mate choice are predicted to maintain genetic variation in the presence of choice for good genes. Received: 8 March 2000 / Revised: 26 August 2000 / Accepted: 4 September 2000