Sexual transmission may drive pair similarity of the cloacal microbiome in a polyandrous species.

All animals host a microbial community within and on their reproductive organs, known as the reproductive microbiome. In free-living birds, studies on the sexual transmission of bacteria have typically focused on a few pathogens instead of the bacterial community as a whole, despite a potential link to reproductive function. Theory predicts higher sexual transmission of the reproductive microbiome in females via the males' ejaculates and higher rates of transmission in promiscuous systems. We studied the cloacal microbiome of breeding individuals of a socially polyandrous, sex-role-reversed shorebird, the red phalarope (Phalaropus fulicarius). We expected (i) higher microbial diversity in females compared to males; (ii) low compositional differentiation between sexes; (iii) lower variation in composition between individuals (i.e. microbiome dispersion) in females than in males; (iv) convergence in composition as the breeding season progresses as a consequence of sexual transmission and/or shared habitat use; and (v) higher similarity in microbial composition between social pair members than between two random opposite-sex individuals. We found no or small between-sex differences in cloacal microbiome diversity/richness and composition. Dispersion of predicted functional pathways was lower in females than in males. As predicted, microbiome dispersion decreased with sampling date relative to clutch initiation of the social pair. Microbiome composition was significantly more similar among social pair members than among two random opposite-sex individuals. Pair membership explained 21.5% of the variation in taxonomic composition and 10.1% of functional profiles, whereas temporal and sex effects explained only 0.6%-1.6%. Consistent with evidence of functional convergence of reproductive microbiomes within pairs, some select taxa and predicted functional pathways were less variable between social pair members than between random opposite-sex individuals. As predicted if sexual transmission of the reproductive microbiome is high, sex differences in microbiome composition were weak in a socially polyandrous system with frequent copulations. Moreover, high within-pair similarity in microbiome composition, particularly for a few taxa spanning the spectrum of the beneficial-pathogenic axis, demonstrates the link between mating behaviour and the reproductive microbiome. Our study is consistent with the hypothesis that sexual transmission plays an important role in driving reproductive microbiome ecology and evolution.

Morph-dependent fitness and directional change of morph frequencies over time in a Dutch population of Common buzzards Buteo buteo.

How genetic polymorphisms are maintained in a population is a key question in evolutionary ecology. Previous work on a plumage colour polymorphism in the common buzzard Buteo buteo suggested heterozygote advantage as the mechanism maintaining the co-existence of three morphs (light, intermediate and dark). We took advantage of 20 years of life-history data collected in a Dutch population to replicate earlier studies on the relationship between colour morph and fitness in this species. We examined differences between morphs in adult apparent survival, breeding success, annual number of fledglings produced and cumulative reproductive success. We found that cumulative reproductive success differed among morphs, with the intermediate morph having highest fitness. We also found assortative mating for colour morph, whereby assortative pairs were more likely to produce offspring and had longer-lasting pair bonds than disassortative pairs. Over the 20-year study period, the proportion of individuals with an intermediate morph increased. This apparent evolutionary change did not just arise from selection on individual phenotypes, but also from fitness benefits of assortative mating. The increased frequency of intermediates might also be due to immigration or drift. We hypothesize that genetic variation is maintained through spatial variation in selection pressures. Further studies should investigate morph-dependent dispersal behaviour and habitat choice.

Drd4 gene polymorphisms are associated with personality variation in a passerine bird.

Polymorphisms in several neurotransmitter-associated genes have been associated with variation in human personality traits. Among the more promising of such associations is that between the human dopamine receptor D4 gene (Drd4) variants and novelty-seeking behaviour. However, genetic epistasis, genotype-environment interactions and confounding environmental factors all act to obscure genotype-personality relationships. Such problems can be addressed by measuring personality under standardized conditions and by selection experiments, with both approaches only feasible with non-human animals. Looking for similar Drd4 genotype-personality associations in a free-living bird, the great tit (Parus major), we detected 73 polymorphisms (66 SNPs, 7 indels) in the P. major Drd4 orthologue. Two of the P. major Drd4 gene polymorphisms were investigated for evidence of association with novelty-seeking behaviour: a coding region synonymous single nucleotide polymorphism (SNP830) and a 15bp indel (ID15) located 5' to the putative transcription initiation site. Frequencies of the three Drd4 SNP830 genotypes, but not the ID15 genotypes, differed significantly between two P. major lines selected over four generations for divergent levels of 'early exploratory behaviour' (EEB). Strong corroborating evidence for the significance of this finding comes from the analysis of free-living, unselected birds where we found a significant association between SNP830 genotypes and differing mean EEB levels. These findings suggest that an association between Drd4 gene polymorphisms and animal personality variation predates the divergence of the avian and mammalian lineages. Furthermore, this work heralds the possibility of following microevolutionary changes in frequencies of behaviourally relevant Drd4 polymorphisms within populations where natural selection acts differentially on different personality types.

Variation in fine-scale genetic structure and local dispersal patterns between peripheral populations of a South American passerine bird.

The distribution of suitable habitat influences natal and breeding dispersal at small spatial scales, resulting in strong microgeographic genetic structure. Although environmental variation can promote interpopulation differences in dispersal behavior and local spatial patterns, the effects of distinct ecological conditions on within-species variation in dispersal strategies and in fine-scale genetic structure remain poorly understood. We studied local dispersal and fine-scale genetic structure in the thorn-tailed rayadito (Aphrastura spinicauda), a South American bird that breeds along a wide latitudinal gradient. We combine capture-mark-recapture data from eight breeding seasons and molecular genetics to compare two peripheral populations with contrasting environments in Chile: Navarino Island, a continuous and low density habitat, and Fray Jorge National Park, a fragmented, densely populated and more stressful environment. Natal dispersal showed no sex bias in Navarino but was female-biased in the more dense population in Fray Jorge. In the latter, male movements were restricted, and some birds seemed to skip breeding in their first year, suggesting habitat saturation. Breeding dispersal was limited in both populations, with males being more philopatric than females. Spatial genetic autocorrelation analyzes using 13 polymorphic microsatellite loci confirmed the observed dispersal patterns: a fine-scale genetic structure was only detectable for males in Fray Jorge for distances up to 450 m. Furthermore, two-dimensional autocorrelation analyzes and estimates of genetic relatedness indicated that related males tended to be spatially clustered in this population. Our study shows evidence for context-dependent variation in natal dispersal and corresponding local genetic structure in peripheral populations of this bird. It seems likely that the costs of dispersal are higher in the fragmented and higher density environment in Fray Jorge, particularly for males. The observed differences in microgeographic genetic structure for rayaditos might reflect the genetic consequences of population-specific responses to contrasting environmental pressures near the range limits of its distribution.

Sources of (co)variation in alternative siring routes available to male great tits (Parus major).

Males of socially monogamous species can increase their siring success via within-pair and extra-pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five-year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as "interactive phenotypes" arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra-pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra-pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multilevel structure of male fertilization routes when studying the evolution of male mating strategies.

Adaptive sleep loss in polygynous pectoral sandpipers.

The functions of sleep remain elusive. Extensive evidence suggests that sleep performs restorative processes that sustain waking brain performance. An alternative view proposes that sleep simply enforces adaptive inactivity to conserve energy when activity is unproductive. Under this hypothesis, animals may evolve the ability to dispense with sleep when ecological demands favor wakefulness. Here, we show that male pectoral sandpipers (Calidris melanotos), a polygynous Arctic breeding shorebird, are able to maintain high neurobehavioral performance despite greatly reducing their time spent sleeping during a 3-week period of intense male-male competition for access to fertile females. Males that slept the least sired the most offspring. Our results challenge the view that decreased performance is an inescapable outcome of sleep loss.

Isolation and characterization of polymorphic microsatellite loci for the northern flicker (Colaptes auratus; Aves).

To investigate the mating system of northern flickers (Colaptes auratus), we developed primers for 14 microsatellite loci and screened them in 68 unrelated adults and their offspring. All markers were highly polymorphic with 9 to +36 alleles per locus. One marker was Z-chromosome linked; one marker exceeded the size standard range and could not be analysed further. We checked the other 12 markers for Mendelian inheritance in 36 broods for which the social parents were known. Seven markers showed evidence for the presence of null alleles, and three of those showed significant deviation from Hardy-Weinberg equilibrium. Markers were generally unlinked.

Convergent evolution of strigiform and caprimulgiform dark-activity is supported by phylogenetic analysis using the arylalkylamine N-acetyltransferase (Aanat) gene.

Alternative hypotheses propose the sister order of owls (Strigiformes) to be either day-active raptors (Falconiformes) or dark-active nightjars and allies (Caprimulgiformes). In an effort to identify molecular characters distinguishing between these hypotheses we examined a gene, arylalkylamine N-acetyltransferase (Aanat), potentially associated with the evolution of avian dark-activity. Partial Aanat coding sequences, and two introns, were obtained from the genomic DNA of 16 species: Strigiformes (four species), Falconiformes (four species), Caprimulgiformes (five species), with outgroups: Ciconiiformes (one species), Passeriformes (one species), and Apterygiformes (one species). Phylogenetic trees derived from aligned, evolutionarily conserved Aanat regions did not consistently recover clades corresponding to orders Strigiformes and Falconiformes but did place a caprimulgiform clade more distant from the strigiform and falconiform species than the latter two groups are to each other. This finding was supported by spectral analysis. The taxonomic distribution of seven intronic indels is consistent with the Aanat derived phylogenetic trees and supports conventional family-level groupings within both Strigiformes and Caprimulgiformes. The phylogenetic analyses also indicate that Caprimulgiformes is a polyphyletic grouping. In conclusion the data support, but do not conclusively prove, the proposal that Falconiformes is the sister order to Strigiformes and therefore, that the dark-activity characteristic of Strigiformes and Caprimulgiformes arose by convergent evolution.