Joseph Haydock

NATAL DISPERSAL IN THE COOPERATIVELY BREEDING ACORN WOODPECKER

Abstract Dispersal data are inevitably biased toward short-distance events, often highly so. We illustrate this problem using our long-term study of Acorn Woodpeckers (Melanerpes formicivorus) in central coastal California. Estimating the proportion of birds disappearing from the study area and correcting for detectability within the maximum observable distance are the first steps toward achieving a realistic estimate of dispersal distributions. Unfortunately, there is generally no objective way to determine the fates of birds not accounted for by these procedures, much less estimating the distances they may have moved. Estimated mean and root-mean-square dispersal distances range from 0.22–2.90 km for males and 0.53–9.57 km for females depending on what assumptions and corrections are made. Three field methods used to help correct for bias beyond the limits of normal study areas include surveying alternative study sites, expanding the study site (super study sites), and radio-tracking dispersers within a population. All of these methods have their limitations or can only be used in special cases. New technologies may help alleviate this problem in the near future. Until then, we urge caution in interpreting observed dispersal data from all but the most isolated of avian populations.

Reproductive roles in the cooperatively breeding acorn woodpecker: incest avoidance versus reproductive competition.

Incest is rare in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus) despite a polygynandrous mating system in which nearly all group members are close relatives. Here we test the relative importance of avoiding matings between close relatives (incest avoidance) and within‐sex competition for breeding opportunities (reproductive competition) in determining the mating system of acorn woodpeckers by examining how reproductive roles change following breeding vacancies. In 83% of cases in which helpers of the same sex were present in the group, reproductive vacancies were resolved when new unrelated immigrants filled the vacancy to the exclusion of resident same‐sex helpers, who generally emigrated or did not breed while they remained in the group. Helpers of the opposite sex, especially when male, were significantly more likely to remain in their natal group and in about half the cases inherited and bred following reproductive vacancies. This result was not explainable by reproductive competition, since the number of immigrants was often less than or equal to the number of same‐sex helpers in the group. Apparent incest resulted in 5% of cases. The time required to resolve reproductive vacancies was significantly longer for groups with helpers of the same sex as the vacancy. These results confirm that both incest avoidance and reproductive competition are important factors determining reproductive roles within groups of this highly social species.

Reproductive skew in the polygynandrous acorn woodpecker

Reproductive skew models, which focus on the degree to which reproduction is shared equally (low skew) or monopolized by a single individual (high skew) within groups, have been heralded as providing a general unifying framework for understanding the factors determining social evolution. Here, we test the ability of optimal skew, or “transactional,” models, which predict the level of skew necessary to promote stable associations of dominants and subordinates, rather than independent breeding, to predict reproductive partitioning in the acorn woodpecker (Melanerpes formicivorus). This species provides a key test case because only a few vertebrates exhibit polygynandry (multiple breeders of both sexes within a group). Contrary to the predictions of the models, joint-nesting females share reproduction more equitably than expected, apparently because egg destruction and the inability of females to defend their eggs from cobreeders eliminate any possibility for one female to control reproduction. For males, however, reproductive skew is high, with the most successful male siring over three times as many young as the next most successful male. Although this result is consistent with optimal skew models, other aspects of male behavior are not; in particular, the reproductively most successful male frequently switches between nests produced by the same set of cobreeders, and we were unable to detect any phenotypic correlate of success. These results are consistent with an alternative null model in which cobreeder males have equal chance of paternity, but paternity of offspring within broods is nonindependent as a consequence of female, rather than male, control.

Shared parentage and incest avoidance in the cooperatively breeding acorn woodpecker

Social groups of acorn woodpeckers (Melanerpesformicivorus) range in size from unaided pairs to 15 adults. Behavioural indicators of mate guarding, assumed incest avoidance and observations of egg‐laying indicate that social organization ranges from monogamous pairs to groups with up to seven male and three female putative cobreeders plus up to 10 nonbreeding helpers. In addition, groups occasionally lack a putative breeder throughout the breeding season. Here we report results from multilocus DNA fingerprinting of 372 nestlings from 123 nests in groups with putative cobreeders of one or both sexes. No extra‐group fertilizations were found. Putative cobreeding males within social groups shared paternity. However, the most reproductively successful male was, on average, almost three times as successful as the next most successful and additional males only occasionally sired offspring. In contrast, cobreeding females shared parentage equally. Helpers never bred incestuously when their opposite‐sex parent (or another relative, such as their uncle) held breeding status in the group. However, during breeding male vacancies, 14 nestlings were produced when helper males bred incestuously with their mother. Both male and female helpers usually became successful cobreeders with their same‐sex parent following replacement of the opposite‐sex breeder(s) by unrelated individuals.

Patterns of reproductive skew in the polygynandrous acorn woodpecker

We compared observed levels of reproductive skew in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus) with those predicted by two alternative transactional models. “Concession” models predict the degree to which parentage is shared assuming that a single dominant is in complete control of reproduction. Alternatively, “restraint” models predict reproductive sharing assuming that the dominant controls only whether subordinates remain in the group but does not control its share of reproduction. Reproductive skew is high among males: on average, the most successful male sires more than three times as many offspring as the next most successful male. Females share parentage equally and have lower constraints on dispersal and lower survival rates compared with males, which is consistent with predictions from the concessions model. Also as predicted by the concessions model, yearly variation in opportunities for dispersal before the breeding season correlates positively with skew. However, in contrast to concessions but consistent with the restraint model, skew decreases with relatedness. Thus, neither model consistently predicts patterns of reproductive skew in this species. We suggest that models of reproductive skew will need to include competitive interactions among potential breeders and mate choice before they will adequately predict patterns of reproductive partitioning in most vertebrate societies.

Variable Helper Effects, Ecological Conditions, and the Evolution of Cooperative Breeding in the Acorn Woodpecker

The ecological conditions leading to delayed dispersal and helping behavior are generally thought to follow one of two contrasting scenarios: that conditions are stable and predictable, resulting in young being ecologically forced to remain as helpers (extrinsic constraints and the habitat saturation hypothesis), or that conditions are highly variable and unpredictable, leading to the need for helpers to raise young, at least when conditions are poor (intrinsic constraints and the hard life hypothesis). We investigated how variability in ecological conditions influences the degree to which helpers augment breeder fitness in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus), a species in which the acorn crop, territory quality, and prior breeding experience all vary in ways that have important effects on fitness. We found that the relationship between ecological conditions and the probability that birds would remain as helpers was variable but that helpers generally yielded greater fitness benefits when ecological conditions were favorable, rather than unfavorable, for breeding. These results affirm the importance of extrinsic constraints to delayed dispersal and cooperative breeding in this species, despite its dependence on a highly variable and unpredictable acorn crop. Our findings also confirm that helpers can have very different fitness effects, depending on conditions, but that those effects are not necessarily greater when breeding conditions are unfavorable.

Demographic consequences of incest avoidance in the cooperatively breeding acorn woodpecker.

The avoidance of breeding with close relatives is an adaptation to inbreeding depression. Unfortunately, inbreeding depression has proved difficult to document or measure in the wild, despite being frequently observed among animals in captivity. We address this problem indirectly by determining the demographic cost of incest avoidance in the cooperatively breeding, polygynandrous acorn woodpecker, Melanerpes formicivorus, following the death or disappearance of all breeders of one sex within a group (a reproductive vacancy). Groups undergoing female vacancies that also contained female nonbreeding helpers experienced significantly lower reproductive success in each of the subsequent 3 years than those in which either no nonbreeding helpers or only male nonbreeding helpers were present, a decrease attributable to incest avoidance between the helper females and the related breeder males in the group. Using a computer simulation combined with a life-table analysis, we estimated that incest avoidance costs the population 9.2-12.1% in overall reproductive potential (measured in fledglings/female) and decreases the population rate of increase by 1.78-2.33%/year. These results suggest the presence, on average, of at least 1.2-1.8 lethal equivalents per individual, a value of the same magnitude as estimated for several other taxa, including humans. Incest avoidance may compound random demographic and environmental events and significantly facilitate the decline of threatened populations even prior to any detrimental effects of inbreeding depression per se. Copyright 1999 The Association for the Study of Animal Behaviour.

Genetic monogamy in single‐male groups of acorn woodpeckers, Melanerpes formicivorus

Acorn woodpeckers have one of the most complex social systems of any bird species. Breeding units range in size from monogamous pairs to groups of 15 birds that include multiple breeding males and females as well as nonreproductive helpers‐at‐the‐nest. Groups form when young remain at their natal nest to help their parents breed or when single‐sex coalitions of siblings disperse to fill a reproductive vacancy on another territory. Plural breeding and helping behaviour are thought to be favoured through indirect fitness benefits for individuals that would otherwise be unable to breed due to a shortage of reproductive vacancies on territories with acorn stores. We report the results of multi‐locus DNA fingerprinting of 51 offspring from 18 nests of 16 socially monogamous pairs of acorn woodpeckers. If socially monogamous females mate outside the pair‐bond, indirect fitness benefits for cobreeders and helpers will be significantly reduced. Monogamous pairs accounted for all but one of the 51 offspring we tested; the single exception was apparently sired by the putative father, but the putative mother was excluded from maternity. Our results indicate that individuals remaining on their natal territories as helpers are generally the genetic offspring of the pair they help. They also suggest that single‐sex coalitions offspring dispersing together from nests of socially monogamous pairs will be full‐siblings.

Genetic monogamy in long-eared owls

We used DNA fingerprinting to study genetic parentage in socially monogamous Long-cared Owls (Asio otus). We detected no extra-pair fertilizations (EPFs) in 59 nestlings from 12 nests. One of these nests was solitary, but the other 11 had from one to five pairs of owls nesting simultaneously within 30 to 250 m. Thus, despite the presumably high potential for extra-pair matings, the Long-cared Owls that we studied were genetically monogamous. In addition, based on low band sharing among adults, we found no evidence that nesting aggregations were composed of close relatives. Genetic monogamy appears to be the rule for socially monogamous raptors. We suggest that the high rate of male parental effort in raptors selects against EPFs because females that engage in extra-pair activities risk losing parental investment by males whose confidence in paternity is reduced owing to the behavior of their mates.

Multilocus minisatellite DNA fingerprinting and cooperative breeding

McRae and Amos (1999) make the valuable point that, when incest has occurred in cooperatively breeding birds, multilocus minisatellite DNA fingerprinting is limited in its ability to resolve parentage. Their general point is a good one, and one that they rightly point out has not been fully appreciated in studies of cooperative breeding. We nonetheless feel that they have overemphasized the problems associated with the application of multilocus minisatellite fingerprinting, as well as the advantages of using single-locus microsatellites. The main difficulty McRae and Amos (1999) identify is that, when an offspring (I) results from an incestuous mating between a mother (M) and her son (S), it will not be possible to exclude the paternal grandfather ( F) from paternity of I, by conventional band-matching analyses. If the son’s fatherF is the dominant male in the group, he may be “assigned” paternity despite the inability to exclude the son S. This will lead to underestimates of the actual rates of incest. This is a valid point worthy of attention. However, it is premature to abandon minisatellite DNA fingerprinting in these applications in favor of microsatellites because (a) except in populations with unusually low genetic polymorphism, it will usually be possible to determine when incest has not occurred (i.e., it will be possible to exclude S when he is not the father); (b) when mother-son incest has occurred, it will often be possible to exclude F by other (bandsharing) analyses, as McRae and Amos (1999) mention (again, the exceptions will be in populations with low genetic polymorphism), and (c) the conditions of low genetic polymorphism under which (a) and (b) represent difficulties can also affect the variability of microsatellite loci. We will remark on each of these points in turn.