Simon C. Griffith

Stable recombination hotspots in birds

Recombination: The birds and the yeast Apes and mice have a specific gene, PRDM9, that is associated with genomic regions with high rates of recombination, called hotspots. In species with PRDM9, hotspots move rapidly within the genome, varying among populations and closely related species (see the Perspective by Lichten). To investigate recombination hotspots in species lacking PRDM9, Singhal et al. examined bird genomes, which lack a PRDM9 gene. They looked closely at the genomes of finch species and found that recombination was localized to the promoter regions of genes and highly conserved over millions of years. Similarly, Lam and Keeney examined recombination localization within yeast, which also lacks PRDM9. They found a similar more-or-less fixed pattern of hotspots. Thus, recombination in species lacking a PRDM9 gene shows similar patterns of hotspot localization and evolution. Science, this issue p. 913, p. 928; see also p. 932 DNA recombination hotspots in birds are localized to gene regulatory sequences and show evolutionary conservation. [Also see Perspective by Lichten] The DNA-binding protein PRDM9 has a critical role in specifying meiotic recombination hotspots in mice and apes, but it appears to be absent from other vertebrate species, including birds. To study the evolution and determinants of recombination in species lacking the gene that encodes PRDM9, we inferred fine-scale genetic maps from population resequencing data for two bird species: the zebra finch, Taeniopygia guttata, and the long-tailed finch, Poephila acuticauda. We found that both species have recombination hotspots, which are enriched near functional genomic elements. Unlike in mice and apes, most hotspots are shared between the two species, and their conservation seems to extend over tens of millions of years. These observations suggest that in the absence of PRDM9, recombination targets functional features that both enable access to the genome and constrain its evolution.

Female extra-pair mating: adaptation or genetic constraint?

Why do females of so many socially monogamous species regularly engage in matings outside the pair bond? This question has puzzled behavioural ecologists for more than two decades. Until recently, an adaptionists point of view prevailed: if females actively seek extra-pair copulations, as has been observed in several species, they must somehow benefit from this behaviour. However, do they? In this review, we argue that adaptive scenarios have received disproportionate research attention, whereas nonadaptive phenomena, such as pathological polyspermy, de novo mutations, and genetic constraints, have been neglected by empiricists and theoreticians alike. We suggest that these topics deserve to be taken seriously and that future work would benefit from combining classical behavioural ecology with reproductive physiology and evolutionary genetics.

Building genetic networks using relatedness information: a novel approach for the estimation of dispersal and characterization of group structure in social animals

Natal dispersal is an important life history trait driving variation in individual fitness, and therefore, a proper understanding of the factors underlying dispersal behaviour is critical to many fields including population dynamics, behavioural ecology and conservation biology. However, individual dispersal patterns remain difficult to quantify despite many years of research using direct and indirect methods. Here, we quantify dispersal in a single intensively studied population of the cooperatively breeding chestnut‐crowned babbler (Pomatostomus ruficeps) using genetic networks created from the combination of pairwise relatedness data and social networking methods and compare this to dispersal estimates from re‐sighting data. This novel approach not only identifies movements between social groups within our study sites but also provides an estimation of immigration rates of individuals originating outside the study site. Both genetic and re‐sighting data indicated that dispersal was strongly female biased, but the magnitude of dispersal estimates was much greater using genetic data. This suggests that many previous studies relying on mark–recapture data may have significantly underestimated dispersal. An analysis of spatial genetic structure within the sampled population also supports the idea that females are more dispersive, with females having no structure beyond the bounds of their own social group, while male genetic structure expands for 750 m from their social group. Although the genetic network approach we have used is an excellent tool for visualizing the social and genetic microstructure of social animals and identifying dispersers, our results also indicate the importance of applying them in parallel with behavioural and life history data.

An empiricist guide to animal personality variation in ecology and evolution

The study of animal personality variation promises to provide significant new insight into the way that behaviour evolves in animals, along with its ecological and evolutionary influences. We strongly advocate more empirical work in this exciting and rapidly expanding research area, but hope that new studies adopt a more hypothesis-driven and/or experimental approach than seems to be usual at the moment. Here we outline what we feel is “good practice” to the many empiricists that are keen on pursuing work in this field. We highlight the substantial body of theoretical work that exists for providing well-reasoned hypotheses, which new empirical studies should be designed to test. Furthermore, using a brief review of existing work on the behavioural ecology of animal personality variation in the zebra finch - one of the more widely used model systems in this field - we stress the importance of understanding the ecology of the chosen study animal, and the problems that are likely to arise by neglecting to identify or account for the structure of behavioural variation that is often likely to occur.

Effects of predation risk on foraging behaviour and group size: adaptations in a social cooperative species

There is a divergence between models examining the evolution of group living in species in which groups are largely based on families and those based on fluid aggregations of nonrelatives. In the former, the onus has been on ecological and demographic factors that select for offspring philopatry; in the latter, the importance of factors such as foraging success and predation risk are more typically emphasized. We examined the association between predation risk and both group size and foraging behaviour in the chestnut-crowned babbler, Pomatostomus ruficeps, a family-living cooperatively breeding bird that does not appear to face classic ecological or demographic constraints on dispersal and breeding. Groups were more likely to encounter, and be attacked by, avian predators when dependent young were present. Large groups were also more likely to encounter a predator, but less likely to be attacked by it, consistent with a benefit of group living through early predator detection or confusion effects. In addition, the average risk of predation for a given individual was reduced in large groups compared to small ones, owing to the dilution effect. That predation might partly select for group living in this species is boosted by findings showing reductions in ground foraging and increases in sentinel behaviour when predation risk was higher. We conclude that predation might represent an important force selecting for sociality in chestnut-crowned babblers, and highlight the need for future studies to consider more explicitly inherent benefits to group living in the evolution of vertebrate cooperative breeding systems.

Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird

Kin selection theory has been the central model for understanding the evolution of cooperative breeding, where non-breeders help bear the cost of rearing young. Recently, the dominance of this idea has been questioned; particularly in obligate cooperative breeders where breeding without help is uncommon and seldom successful. In such systems, the direct benefits gained through augmenting current group size have been hypothesized to provide a tractable alternative (or addition) to kin selection. However, clear empirical tests of the opposing predictions are lacking. Here, we provide convincing evidence to suggest that kin selection and not group augmentation accounts for decisions of whether, where and how often to help in an obligate cooperative breeder, the chestnut-crowned babbler (Pomatostomus ruficeps). We found no evidence that group members base helping decisions on the size of breeding units available in their social group, despite both correlational and experimental data showing substantial variation in the degree to which helpers affect productivity in units of different size. By contrast, 98 per cent of group members with kin present helped, 100 per cent directed their care towards the most related brood in the social group, and those rearing half/full-sibs helped approximately three times harder than those rearing less/non-related broods. We conclude that kin selection plays a central role in the maintenance of cooperative breeding in this species, despite the apparent importance of living in large groups.

Parental care in wild and captive zebra finches : measuring food delivery to quantify parental effort

Although the zebra finch, Taeniopygia guttata, has been a very important model system for the study of intrafamilial conflict and parental strategies, a detailed understanding of the variation in parental effort that can occur both within and between pairs is lacking. In part this is because many different methods have been used by individual studies to quantify parental care (i.e. nest visit rate, time in the nest and number of feeds per visit), but these have not directly been compared. We used nestbox cameras to monitor parental visit rate and the distribution of food among the nestlings in domestic, captive wild and wild free-living zebra finches. The percentage of nest visits by parents in which they fed the nestlings was consistent, with multiple feeds to different nestlings occurring within a single visit. The quantity of food delivered and its distribution among the nestlings, however, varied greatly both within and between broods. The number of regurgitations a brood received correlated significantly with the number of individual feeds when accounting for environment, but not with nest visit rate or the duration of time parents spent in the nestbox. In captive conditions, parents visited the nest at twice the rate of wild free-living birds, overall providing nestlings with twice the amount of food. Captive conditions also led to food distribution becoming less equitable among the brood, owing to changes in the number of regurgitations per individual feed and the number of overall feeds per nest visit.

Constrained mate choice in social monogamy and the stress of having an unattractive partner

In socially monogamous animals, mate choice is constrained by the availability of unpaired individuals in the local population. Here, we experimentally investigate the physiological stress endured by a female (the choosy sex) when pairing with a non-preferred social partner. In two experimental contexts, female Gouldian finches (Erythrura gouldiae) socially paired with poor-quality mates had levels of circulating corticosterone that were three to four times higher than those observed in females that were paired with preferred mates. The elevated level of this stress hormone in response to partner quality was observed within 12 h of the experimental introduction and maintained over a period of several weeks. Our findings demonstrate the extent of intra-individual conflict that occurs when individuals are forced to make mate-choice decisions that are not perfectly aligned with mate-choice preferences. The elevated level of corticosterone also suggests a mechanistic route through which females might adaptively manage their responses to intersexual conflict over reproductive investment.

The Adaptive Significance of Provisioning and Foraging Coordination between Breeding Partners

Sexual conflict over parental care relies on the fundamental assumption that parents do not share the cost of their partner’s effort on future reproduction. However, this is unlikely to be true whenever partners breed together more than once. In that case, individuals should try to optimize the cost and benefits for the pair, rather than only for themselves. Here we seek to establish whether the synchronization of parents’ provisioning visits to the nest could fulfill this function. We conducted a brood-size manipulation experiment on wild zebra finches to test whether nest visit synchrony was flexible and beneficial for nestlings’ growth, while controlling for the confounding effects of pair “quality” and synchrony away from the nest during foraging. Using a network of readers to track parents at nests and feeding stations, we found that nest visit synchrony responded directly to the brood manipulation and increased with brood size. Synchrony at the nest and while foraging were correlated, but the latter better predicted nestling mass, possibly because it was associated with more regular provisioning patterns. Our findings suggest that parental coordination could indeed play an important role in partners’ investment decisions, underpinning the evolution of the most prominent mating system in birds.

Incubation behaviour and hatching synchrony differ in wild and captive populations of the zebra finch

Hatching asynchrony is widespread in birds laying clutches containing multiple eggs, yet is seemingly paradoxical as the age and size hierarchies result in asymmetric sibling competition and low survival prospects for late-hatched nestlings. We examined the causes of variation in hatching asynchrony between broods of zebra finch, Taeniopygia guttata, in three environments: domesticated, captive wild and wild free-living. We found that broods of both domesticated and wild birds taken into captivity hatched more asynchronously than wild free-living broods. This was directly attributable to both male and female parents of domesticated and captive wild broods initiating incubation as soon as the first egg was laid as opposed to when the clutch was virtually complete in wild free-living broods. Wild free-living birds that were transferred to captive environments immediately switched to the incubation onset behaviour seen in domesticated birds, thereby demonstrating a previously unsuspected level of intraspecific plasticity in incubation behaviour. This finding suggests that something about the captive environment is driving the early onset of incubation and contributing to an elevated level of hatching asynchrony in captive birds. Across all populations and environments males contributed almost equally to incubation, and the onset of incubation by males was highly coordinated with that of their partner.