Genetic monogamy in the common loon (Gavia immer)

We conducted behavioral observations and genetic analysis on breeding pairs of common loons in the upper Great Lakes region from 1993 through 1995 to look for behavioral evidence of extrapair copulations (EPCs) and to determine parentage of young. Pairs remained close to each other (usually within 20 m) during the pre-laying period, leaving little opportunity for EPCs to occur. Males and females both maintained physical proximity by approaching each other when they became separated. Copulations were obvious but infrequent, occurring about once every other day during the pre-laying period. Multilocus DNA fingerprinting was consistent with behavioral findings: 58 young from 47 different families were all genetic offspring of parents that raised them. Perfect genetic monogamy (genetic parentage of young by parents that rear them) in loons might arise as a consequence of the need for vigorous territorial defense to prevent territorial takeover. Received: 8 August 1996 / Accepted after revision: 22 March 1997     

Multiple paternity in the cooperatively breeding fish <Emphasis Type="Italic">Neolamprologus pulcher</Emphasis>

In cooperative breeders, mature males may compete for fertilizations. In this study, we measured the degree of multiple paternity in a natural population of a cooperatively breeding fish. Neolamprologus pulcher (Perciformes: Cichlidae) is a highly social cichlid endemic to Lake Tanganyika. We used highly variable microsatellite loci to survey 12 groups with an average number of 10.6 brood care helpers per group and a total of 43 offspring (mean 3.6 per brood). In 11 of 12 groups, all young were assigned to the dominant female. The dominant male sired all offspring in three groups, part of the offspring in four groups, and in five groups, he had no paternity at all. In total, 44.2% of young were not fathered by the current male territory owner. Multiple paternity was found in 5 of 12 broods (41.7 %), with 8 of 35 young (22.9 %) being sired by males other than the respective territory owners. This is an exceptionally high rate of extra-pair paternity among cooperatively breeding vertebrates. Neither helpers present in these territories during collection nor neighbouring males were unequivocally assigned to have sired these extra-pair young. However, behavioural observations suggest that male helpers may have produced these young before being expelled from the territory in response to this reproductive parasitism. We discuss these results in the light of reproductive skew theory, cooperative breeding in vertebrates and alternative reproductive tactics in fish.     

No evidence for acoustic mate-guarding in duetting buff-breasted wrens (Thryothorus leucotis)

There are few empirical tests of the acoustic mate-guarding hypothesis for the function of duetting in birds. This hypothesis states that when females are fertile, males initiate many songs or answer most of their mates solo songs to form duets and repel rival males seeking extra-pair copulations. We tested the hypothesis by comparing song initiation and answer rates of males and females in socially monogamous buff-breasted wrens (Throthorus leucotis) during pre-fertile and fertile periods. During pre-fertile periods, males often sang for short periods before being answered by their mates, yet first duets were formed earlier relative to dawn and more duets were given during the dawn chorus on pre-fertile than fertile mornings. Males initiated more songs during pre-fertile than fertile periods, whereas there was no difference between stages in female song initiation rates. The proportion of songs answered by individuals of both sexes did not differ between breeding stages. Other mate-guarding behaviours, such as frequent copulation and maintaining close proximity to mates when fertile, did not appear to be important in this species, as no copulations were observed and there was no difference in the time pairs spent in close proximity when females were fertile or not. Parentage analysis revealed that only 3% of 31 broods had young that were likely the result of extra-pair paternity. These findings do not support the acoustic mate-guarding hypothesis, and suggest that the low rate of extra-pair paternity in buff-breasted wrens was maintained without the use of acoustic or traditional paternity guards.Communicated by R. Gibson     

The genetic mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular inquiry

In the pipefish Syngnathus typhle as in other species of Syngnathidae, developing embryos are reared on the male's ventral surface. Although much laboratory research has been directed toward understanding sexual selection in this sex-role-reversed species, few studies have addressed the mating behavior of S. typhle in the wild, and none has capitalized upon the power of molecular genetic assays. Here we present the first direct assessment of the genetic mating system of S. typhle in nature. Novel microsatellite loci were cloned and characterized from this species, and employed to assay entire broods from 30 pregnant, field-captured males. Genetic analysis of 1340 embryos revealed that 1–6 females (mean = 3.1) contributed to each brooded clutch, the highest rate of multiple maternity yet documented in any pipefish. Evidence of multiple mating by females was also detected. Thus, this population of S. typhle displays a polygynandrous mating system, a finding consistent with previous field and laboratory observations. Our results, considered together with similar studies of other syngnathid species, provide preliminary support for the hypothesis that the genetic mating system is related to the evolution of sexual dimorphism in the fish family Syngnathidae. Received: 19 January 1999 / Received in revised form: 15 April 1999 / Accepted: 9 May 1999     

Kin associations and direct vs indirect fitness benefits in colonial cooperatively breeding sociable weavers Philetairus socius

Indirect fitness benefits are believed to be an important force behind the evolution of cooperative breeding. However, helpers may associate with their relatives as a result of delayed dispersal, hence, kin associations might be a consequence of demographic viscosity rather than active choice. In addition, recent studies showed that helpers may have access to reproduction therefore direct benefits might also play an important role. Here, we investigate the possible roles of direct genetic benefits and kin associations on helping behavior in the sociable weaver Philetairus socius, a colonial and cooperatively breeding passerine. We used a microsatellite-based genotyping method to describe the genetic structure within nests and colonies. Within a colony, we found considerable genetic structure between males but not females. Sociable weaver colonies have several nests that are simultaneously active, giving individuals a choice of associating with a range of first-order kin to unrelated individuals. Helpers were significantly more related to the young in the helped nests than in other nests of the colony, suggesting an active choice for associating with kin. The helpers were generally offspring or first-order relatives of one (50%) or both (43%) breeders, although more infrequently, seemingly unrelated individuals also helped (7%). We found no supporting evidence of extrapair parentage and hence no direct genetic gains from helping in our population. This strong reproductive skew is contrary to theoretical models predicting conflicts over reproduction in stepfamilies. We discuss whether female decisions and/or other direct benefits of remaining in kin associations or helping might explain the high skew observed.     

Red-winged blackbird parental investment following brood parasitism by brown-headed cowbirds: is parentage important?

Parental investment by red-winged blackbirds (Agelaius phoeniceus) in response to natural and experi‐mental parasitism by brown-headed cowbirds (Molothrus ater), and in response to freeze-dried, female cowbird mounts presented near redwing nests during the egg-laying period was measured. Two measures of redwing parental investment were used: nest defense effort toward a model predator, and rate of feeding nestlings. There were no significant differences in levels of parental investment among unparasitized nests, naturally parasitized nests, or experimentally parasitized nests. Similarly, parental investment did not differ between redwings that were exposed to the cowbird mount and those that were not exposed to the mount, or among redwings exposed to the cowbird mount at different distances from the nest. This suggests that red-winged blackbirds do not recognize when they have been parasitized, and hence do not associate parasitism with a decrease in their parentage, or that parentage is not an important predictor of parental investment in this species. Received: 24 January 1997 / Accepted after revision: 7 June 1997     

Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses

It is suggested that some fish of the genus Julidochromis, substrate-brooding Tanganyikan cichlids with biparental care, breed cooperatively with helpers. We studied the social system of J. ornatus in the wild and analysed genetic parentage using microsatellites. Within the studied population three patterns of social system were identified: monogamous pairs (61%, 44 of 72 groups), pairs with helpers (29%, 21), and polygamous harems with helpers (controlled by either a large female or large male owner; 10%, 7). In cooperatively breeding groups, the number of helpers at each nest ranged from 1 to 6 (median 1), and male helpers were more numerous than female helpers. In both sexes, the body size was different among individuals of different social status (harem owner > breeder > helper). Helpers and harem owners of both sexes exhibited brood defence although its frequency was low. The molecular analysis revealed that (1) the helpers were mostly unrelated to dominant breeders, (2) many helpers of both sexes contributed genetically to the next generations, (3) male helpers had high siring success (41% of young in total), and (4) large young unrelated to group members were detected at 30% of observed nests, which may be due to breeder (or helper) replacements and immigration of young. We discuss the implications of these results for understanding the complex social system of this species, especially the low reproductive skew in comparison with other cooperatively breeding cichlids.     

Genetic evidence for mixed parentage in nests of the emu (Dromaius novaehollandiae)

Parentage in emus (Dromaius novaehollandiae) was examined by microsatellite analysis using four independent loci. Of 106 chicks sampled in one breeding season from 18 nests, 54 (51%) were not fathered by the nesting male, 12 (11%) were not from the observed mate of the sitting male, and 9 (8%) represented intra-specific brood parasitism, having no alleles in common with either nest parent. Some males (11%) fathered all chicks in their nests, but the majority showed high levels of cuckoldry. Those males commencing incubation earliest in the season tended to have the highest levels of paternity in their own nests. These results reveal a high frequency of extra-pair fertilisations and resultant cuckoldry in a predominantly socially monogamous bird and support recent reports which have described the emu mating system as a complexity of polyandrous, promiscuous and monogamous behaviour. Parentage assignment of chicks resulting from extra-pair fertilisations revealed an evenly scattered pattern of paternity that did not show any particular male dominance in reproductive success. These results lead to a reassessment of behavioural observations of emus, the consequences of parentage distribution, and theories about mating systems and sexual selection. The frequency of extra-pair copulations and intra-specific brood parasitism suggests patterns of descent that differ greatly from those implied by social monogamy. Received: 27 November 1999 / Received in revised form: 8 January 2000 / Accepted: 8 February 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     

Multi-locus DNA fingerprinting supports genetic monogamy in Florida scrub-jays

Extensive behavioural and pedigree data on a colour-marked population of Florida scrub-jays (Aphelocoma coerulescens) suggested that this cooperatively breeding species is monogamous, with extremely rare exceptions in which males have two mates. We used multi-locus DNA fingerprinting to test these observations by determining genetic parentage. Despite restricted dispersal and high relatedness between behavioural parents and non-breeding members of the group, DNA fingerprints provided sufficient variability to determine parentage unambiguously in almost all cases. We found no evidence of extra-pair fertilisation of females or egg dumping, and confirmed a suspected case of polygyny in which a mother and daughter laid and incubated in the same nest. Our results confirm that detailed behavioural data allow accurate assignment of genetic parentage in this species. In Florida scrub-jays, large territory size may limit opportunities for cuckoldry, and persistent intense competition for limited breeding space may lead to low variance in the quality of established male breeders. These factors would reduce both the opportunity for, and benefits of engaging in extra-pair fertilisations. Delayed dispersal and cooperative breeding in this species have not evolved as avenues for direct reproduction by unpaired individuals. Received: 25 May 1998 / Accepted after revision: 26 June 1998