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     

Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets

Recent models of the evolution and dynamics of family structure in cooperatively breeding vertebrates predict that the opening of breeding vacancies in cooperatively breeding groups will result in (1) dispersal movements to fill the reproductive position, and (2) within-group conflict over access to reproduction. We describe the behavioral and demographic changes that followed the creation of breeding vacancies in three wild groups of cooperatively breeding common marmosets (Callithrix jacchus). Replacement of the breeding female was rapid when no adult females remained in the group, but did not occur for several months when other adult females were present. Aggression of adult animals towards same-sex potential immigrants was associated with a period of reduced affiliation, increased intragroup agonism, no intragroup sexual behavior, and frequent extragroup copulations. This ended with the fissioning of groups along sexual lines. After replacement, multiple males copulated with multiple females and vice versa, with no increases in sexually related aggression. Female-female conflict was resolved through infanticide. The lack of direct conflict between males is consistent with cooperative polyandry. After a breeding vacancy appeared, marmoset groups showed conflict of interests among group members similar to those shown by cooperatively breeding birds, but they used different behavioral mechanisms to resolve those conflicts. Our data provide important evidence from a cooperatively breeding mammal to support Emlen’s model for the evolution of vertebrate families, but they suggest that species-specific inter- and intrasexual competitive strategies should be considered before the model can be applied to other cooperatively breeding vertebrates. Received: 23 November 1999 / Received in revised form: 28 March 2000 / Accepted: 1 April 2000     

Extra-pair paternity uncommon in the cooperatively breeding bicolored wren

We investigated parentage using multilocus DNA fingerprinting for 222 juveniles produced during 99 group-years in the bicolored wren Campylorhynchus griseus, a cooperatively breeding bird of the Venezuelan savanna. Young adult bicolored wrens (auxiliaries) remain in their natal territories and substantially enhance the production of young there. We have previously used behavioral indicators of dominance by a single male/female pair (principals) to infer breeding status, resulting in the commonly applied model of helping in which current fitness accrues to auxiliaries only indirectly, in proportion to their relatedness to the principals and the effect of their assistance on breeding success. Our parentage analysis has demonstrated that 8.6% of the juveniles found on territories were not produced by the principal pair. Parentage of 4.1% of the juveniles was completely outside the social group; these appear to result from early dispersal of juveniles rather than from brood parasitism, most likely resulting from breakup of nearby groups. Principal females mated outside of their group (2.3%), or with an auxiliary male (2.3%), in the remaining cases of parentage outside the principal pair. No matings were detected between close relatives (e.g. mother-son); matings detected between the principal female and an auxiliary male followed a typical replacement of the principal female by an unrelated immigrant female. Our finger-printing results indicate that: (1) current fitness benefits accruing to most auxiliaries do not exceed their likely reproductive success had they dispersed successfully to a breeding position; (2) nearly all wren mating is monogamous and (3) behavioral dominants (especially females) can monopolize breeding. Received: 23 September 1994/Accepted after revision: 10 June 1995     

Delayed breeding in the cooperatively breeding Florida scrub-jay (Aphelocoma coerulescens): inhibition or the absence of stimulation?

To determine whether fundamental differences exist in the reproductive physiology of breeder and nonbreeder Florida scrub-jays (Aphelocoma coerulescens), we compared plasma levels of testosterone (T) and luteinizing hormone (LH) in males, and estradiol (E₂) and LH in females. Although male breeders had higher overall T and larger testes, nonbreeders’ T paralleled that of breeders, and their testes were more than an order of magnitude larger than regressed testes. Breeder and nonbreeder males had equivalent baseline LH, and equivalent changes in LH following a gonadotropin-releasing hormone (cGnRH-I) challenge. The T, LH and GnRH challenge data indicate that nonbreeder males have functional hypothalamo-pituitary-gonadal (HPG) axes. We found no hormonal evidence of inbreeding suppression in males: nonbreeders that did not live with their mothers and those that did had similar T. Male nonbreeders that were exposed to E₂-implanted females had higher T than did controls, suggesting that the lack of within-pair stimulation is a key factor in whether an individual delays breeding. Female nonbreeders had E₂ titres equal to or higher than breeders and neither basal LH nor LH following GnRH challenge differed by breeding status. Nonbreeders’ ovarian follicles were smaller than breeders’, but were larger than they would be during the non-breeding season. These data suggest that nonbreeders were primed for breeding and were simply waiting for an opportunity or a required stimulus. Female nonbreeders that lived in a territory with an unrelated male breeder had significantly higher E₂ than those that remained with their fathers. Similarly, nonbreeders that were captured away from their home territories had elevated E₂. However, nonbreeders that lived with their fathers had E₂ that was equivalent to breeding females, suggesting that inbreeding avoidance may not be the primary factor leading to delayed breeding in females. Received: 13 June 1995 /Accepted after revision: 27 April 1996     

Genetic evidence for monogamy in the cooperatively breeding red-cockaded woodpecker

We examined the genetic relationship among putative parents, offspring, and helpers in 224 red-cock-aded woodpeckers (Picoides borealis) from the Sandhills of North Carolina. Comparison of DNA similarity with a pedigree constructed from 3,823 individually-marked birds observed from 1979 to 1992 provided verification of observed relatedness in the sampled population (R ² = 0.87, df = 14, P < 0.001). In this population, breeding pairs may or may not have helpers, most of which are males that remain on their natal territory. Our sample included helpers assisting their parents, helpers assisting a related male and an unrelated female, and helpers assisting an unrelated pair. Band by band comparison and examination of similarity among DNA profiles indicated that all offspring from non-helped nests were sired by their putative parents (n = 28 families). Similarly, all but one offspring in helped nests were also sired by their putative parents (n = 16 families). In the exceptional case, the offspring evidently was sired by a male external to the group. Analysis of similarity values supported the conclusion that matings by helpers or extra-group males are rare or non-existent. Our results indicate that in this species advantages gained by individuals remaining on their natal territories as helpers do not generally include siring offspring. Correspondence to: S. Haig     

Genetic evidence for monogamy in the cooperatively breeding red-cockaded woodpecker

We examined the genetic relationship among putative parents, offspring, and helpers in 224 red-cockaded woodpeckers (Picoides borealis) from the Sandhills of North Carolina. Comparison of DNA similarity with a pedigree constructed from 3,823 individually-marked birds observed from 1979 to 1992 provided verification of observed relatedness in the sampled population (R ² = 0.87,df = 14,P<0.001). In this population, breeding pairs may or may not have helpers, most of which are males that remain on their natal territory. Our sample included helpers assisting their parents, helpers assisting a related male and an unrelated female, and helpers assisting an unrelated pair. Band by band comparison and examination of similarity among DNA profiles indicated that all offspring from non-helped nests were sired by their putative parents (n = 28 families). Similarly, all but one offspring in helped nests were also sired by their putative parents (n = 16 families). In the exceptional case, the offspring evidently was sired by a male external to the group. Analysis of similarity values supported the conclusion that matings by helpers or extra-group males are rare or non-existent. Our results indicate that in this species advantages gained by individuals remaining on their natal territories as helpers do not generally include siring offspring. Correspondence to: S. Haig     

Siblicide in the cooperatively breeding laughing kookaburra (Dacelo novaeguineae)

I describe siblicide in the laughing kookaburra (Dacelo novaeguineae), a reverse size-dimorphic, cooperatively breeding kingfisher. Clutches were usually of three eggs, and nestlings hatched asynchronously, with intervals of 2–72 h between successive eggs. Siblicide occurred in two temporally and mechanistically distinct episodes. The youngest nestling died in one-third of all nests within days of hatching as a result of aggression from its elders. Kookaburra nestlings attacked each other using a hook on their upper beak – a rare example of a morphological specialisation for sibling rivalry. In one-fifth of all nests, the youngest nestling starved to death much later, without overt aggression, when nestling growth rates were highest. I examined the effects of food availability and competitive disparities between nestlings on the incidence of both types of siblicide. The probability of late, starvation-mediated mortality was negatively correlated with the number of male helpers. Early, aggressively mediated siblicide occurred in nests characterised by a suite of correlated variables that I call the ”kookaburra siblicide syndrome”: (1) no male helpers attended the nest, (2) the third-hatched nestling was much smaller than the second-hatched nestling, (3) the first and second nestling to hatch were male and female, respectively, and (4) there was a short hatch interval between the first two nestlings. The kookaburra siblicide syndrome variables could be inter-correlated if they were all related to the female’s condition at the onset of incubation. Females in poorer condition may be less likely to have male helpers, more likely to lay small third eggs, and more likely to hatch the first two eggs relatively synchronously because of nutritional constraints during the onset of incubation. These females may further promote siblicide by modifying the sexes of the first two nestlings. If a female hatches soon after an older but eventually smaller brother, dominance between the first two nestlings could be destabilised. I suggest this leads to escalated aggression in the nest and the death of the third nestling, which is least able to defend itself. Received: 17 December 1999 / Received in revised form: 8 May 2000 / Accepted: 20 May 2000     

Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus)

Lactation imposes substantial physiological costs on mothers and should therefore not be directed towards foreign offspring. Such allonursing, however, is common in mammal species that share roosts. Hypotheses to explain allonursing among such plural breeders include misdirected parental care, milk evacuation, brood parasitism, reciprocity, and kin selection. The necessary behavioral data, in combination with data on kinship and kin recognition, have rarely been available to distinguish among these explanations, however. In this study, we provide evidence for cooperative nursing and adoption by plural-breeding females in a nocturnal primate, the gray mouse lemur (Microcebus murinus), in which females forage solitarily during the night, but form day-time sleeping groups with one to two other females. We observed 34 resident females in an 8 ha study area in Kirindy Forest, Madagascar, over three consecutive annual breeding seasons and determined genetic relationships among all members of this population. Five sleeping groups of adult females were filmed inside their roosts during one breeding season after females gave birth. The composition of groups changed substantially across years, but they always consisted of close maternal relatives. All females within a group gave birth to one to three infants. They regularly transferred only their own offspring among roosting sites, demonstrating an ability to discriminate between their own and other’s offspring, but they regularly groomed and nursed related offspring other than their own and adopted related dependent young after their mother’s death. Kin selection may therefore be the main selective force behind cooperative breeding among these closely related females with a high mortality risk, providing each of them with family insurance.     

Delayed dispersal as a potential route to cooperative breeding in ambrosia beetles

Xyleborini are a species-rich tribe of ambrosia beetles, which are haplodiploid and typically mate among siblings within their natal brood chamber. Several characteristics of this tribe would predict the evolution of higher levels of sociality: high genetic relatedness within galleries due to inbreeding, high costs of dispersal and the potential benefit of cooperation in brood care within the natal gallery (e.g. by fungus gardening, gallery extension, offspring feeding and cleaning). However, information on the social system of these beetles is very limited. We examined the potential for cooperative breeding in Xyleborinus saxeseni by monitoring dispersal in relation to brood size and composition. Results show that adult female offspring delay dispersal despite dispersal opportunities, and apparently some females never disperse. The females’ decision to stay seems to depend on the presence of eggs and dependent siblings. We found no indication that female offspring reproduce in their natal gallery, as colonies with many mature daughters do not contain more eggs than those with few or no daughters. There is a significant positive relationship between the number of females present and the number of dependent siblings (but not eggs), which suggests that cooperative brood care of female offspring raises colony productivity by improving survival rates of immatures. Our results suggest that cooperative breeding is likely to occur in X. saxeseni and possibly other xyleborine species. We argue that a closer look at sociality within this tribe may yield important information on the factors determining the evolution of cooperative breeding and advanced social organization.     

Relatedness, polyandry and extra-group paternity in the cooperatively-breeding white-browed scrubwren (Sericornis frontalis )

We used DNA fingerprinting to examine the genetic parentage and mating system of the cooperatively breeding white-browed scrubwren, Sericornis frontalis, in Canberra, Australia. Our analyses revealed a remarkable variety of mating tactics and social organization. Scrubwrens bred in pairs or multi-male groups that consisted of a female and two or more males. Females were always unrelated to the pair male or alpha (dominant) male. Among multi-male groups we found three different mating tactics. Firstly, when alpha and beta (subordinate) males were unrelated, they usually shared paternity in the brood. This resulted in both males gaining reproductive benefits directly. Secondly, when beta males were not related to the female but were related to the alpha males, beta males sired offspring in some broods. In this situation, beta males gained reproductive benefits both directly and potentially indirectly (through the related alpha male). Thirdly, when beta males were related to the female or both the female and alpha male, they remained on their natal territory and did not sire any offspring. Thus beta males gained only indirect reproductive benefits. Overall, when group members were related closely, the dominant male monopolized reproductive success, whereas when the members were not related closely the two males shared paternity equally. This positive association between monopolization of reproduction and relatedness is predicted by models of reproductive skew, but has not been reported previously within a single population of birds. Other cooperatively breeding birds with both closely related and unrelated helpers may show a similar variety of mating tactics. Finally, we found that extra-group paternity was more common in pairs (24% of young) than in multi-male groups (6%), and we discuss three possible reasons for this difference. Received: 21 May 1996 / Accepted after revision: 14 December 1996     

Helpers and egg investment in the cooperatively breeding acorn woodpecker: testing the concealed helper effects hypothesis

In cooperatively breeding acorn woodpeckers (Melanerpes formicivorus), helper males have a large positive effect on fledging success in good acorn crop years but only a small positive effect in poor acorn crop years, while helper females exhibit the opposite pattern. Based on these findings, we tested the “concealed helper effects” hypothesis, which proposes that laying females reduce investment in eggs (with respect to their size, number, or quality) in a way that confounds helper effects and results in an absence of a relationship between helpers and breeding success. Results generally failed to support the hypothesis. Mean egg size was positively related to temperatures during the 10 days prior to egg-laying and negatively related to the food supply as indexed by the prior fall’s acorn crop, but there were no significant differences vis-à-vis helpers except for interactions with the acorn crop that only partly corresponded to those predicted. With respect to clutch size, females laid larger clutches when assisted by female helpers, opposite the pattern predicted. Although our results suggest that egg size is adjusted to particular ecological circumstances, we conclude that neither egg nor clutch size is adjusted in a way that confounds the apparent effects of helpers, as proposed by the concealed helper effects hypothesis.     

Helpers in colonial cooperatively breeding sociable weavers <Emphasis Type="Italic">Philetairus socius</Emphasis> contribute to buffer the effects of adverse breeding conditions

Some studies on the effects of helpers in cooperatively breeding vertebrates show a positive effect of helper presence on reproductive output whereas others find no effect. One possibility for this discrepancy is that helpers may have a positive effect when breeding conditions are adverse, while their effect might go unnoticed under good conditions. We investigate this hypothesis on sociable weavers Philetairus socius, a colonial cooperatively breeding passerine that inhabits a semi-arid region where breeding conditions vary markedly. We used multivariate mixed models to analyse the effect of helpers on reproduction under contrasting environmental and social conditions while controlling for parental and colony identity. We found that reproductive success in sociable weavers was primarily influenced by nest predation and rainfall. In addition, colony size was negatively associated with hatching and fledging success and number of young fledged per season. Helpers had a less prominent but significant influence on feeding rates and reproductive outcome. In agreement with expectations, the presence of helpers counteracted some of the negative effects of breeding in periods of low rainfall or in large colonies and was also associated with an increased number of young fledged per season. Our results illustrate that the effect of helpers might be detectable mostly under unfavourable conditions, but can contribute to improve reproductive performance in those situations.     

Testing the ability of males and females to respond to altered songs in the dueting green lacewing, Chrysoperla plorabunda (Neuroptera: Chrysopidae)

Green lacewings in the carnea group of Chrysoperla engage in species-specific heterosexual duets using low-frequency substrate-borne signals. Within each species, both sexes sing nearly identical songs. Songs are the principal barriers to hybridization between sympatric species in the complex. Here, we investigated the responsiveness of males and females of Chrysoperla plorabunda to synthesized, prerecorded songs that differed from the species mean in the period between repeated volleys of abdominal vibration. We tested 15–16 males and 15–16 females using playbacks of two signals that gradually increased or decreased in volley period, starting at the species mean. We found that (1) duets during courtship are accurate, interactive, and adjustable by each participant; (2) in staged duets, both sexes respond best to song tempos near the mean volley period of their population, but can nonetheless maintain duets with signals of nearly twice, or half, the normal volley period; (3) individuals fine-tune their adjustments to signals of different volley periods by changing their own volley duration and latent period, or less often by inserting extra volleys or skipping every other volley; (4) males are significantly better at matching signals of changing tempo than females; and (5) the range of song responsiveness of C. plorabunda does not overlap the natural range of volley periods found in Chrysoperla adamsi, an acoustically similar sibling species, thus reaffirming strong behavioral isolation. In sum, the precise, almost unbreakable heterosexual duets characteristic of song species of the carnea group result from tight mutual feedback between partners. Effective reproductive isolation between species can be based on song differences alone.     

Who cares? Individual contributions to pup care by breeders vs non-breeders in the cooperatively breeding banded mongoose (<Emphasis Type="Italic">Mungos mungo</Emphasis>)

Knowledge of the investment rules adopted by breeders and non-breeders, and the factors that affect them, is essential to understanding cooperative breeding as part of a life-history tactic. Although the factors that affect relative contributions to care of young have been studied in some cooperative bird species, there is little data on mammals, making coherent generalisations within mammals and across taxa difficult. In this study, we investigate individual contributions to pup escorting, a strong predictor of offspring provisioning, in the banded mongoose (Mungos mungo), a cooperatively breeding mammal in which reproductive skew is low. Contributions by those under a year old (which virtually never breed) increased with age and body weight but were generally low. Among older age classes (yearlings and adults), individuals that had not bred in the current litter generally contributed less to escorting than those that had bred (with the exception of yearling males). In addition, females that did not breed reduced their investment if they were heavy presumably because such females are more likely to breed in the following event and benefit from saving resources for this. The generally greater contributions by breeders in banded mongooses contrast with the recent findings in meerkats (Suricata suricatta), another obligatorily cooperative mongoose with similar group size but wherein reproductive skew is high. Our results suggest that relative contributions by breeders vs non-breeders are not dependent on group size but on the ratio of breeders to carers and the probability that non-breeders will breed in the near future.     

Exposing males to female scent increases the cost of controlling <Emphasis Type="Italic">Salmonella</Emphasis> infection in wild house mice

Secondary sexual characters often provide indicators of a male’s resistance to infectious diseases to rivals and potential mates, but it is unclear why. It is often suggested that males honestly signal their health due to energetic and other physiological trade-offs between investing into secondary sexual traits vs resistance to infectious diseases. Our aim was to determine whether such a trade-off exists using wild-derived male house mice (Mus domesticus). We exposed male mice to female scent, a manipulation that induces elevations in testosterone concentration and the expression of a variety of testosterone-mediated secondary sexual traits, and tested whether this sexual stimulation impaired the males’ ability to resolve or cope with an experimental infection (Salmonella enterica). We kept the males on a controlled diet to prevent them from compensating by eating more food. We found that sexually stimulated males were able to control bacterial growth as effectively as sham-stimulated controls; however, to do so, they lost more body mass during infection compared to the controls. In contrast, we found no evidence that sexual stimulation reduced the body mass of uninfected male mice. These results indicate that males’ responses to female odor are not immunosuppressive per se, yet they increase the energetic costs of controlling infection. Our findings support the idea that there is a physiological trade-off between secondary sexual signaling vs resistance to infectious diseases and suggest that studies using only immunocompetence assays might fail to detect such energetic trade-offs. We dedicate this paper to the late Professor Chris Barnard who conducted pioneering research on this topic.