Neurogenomic landscape associated with status-dependent cooperative behaviour.

The neurogenomic mechanisms mediating male-male reproductive cooperative behaviours remain unknown. We leveraged extensive transcriptomic and behavioural data on a neotropical bird species (Pipra filicauda) that performs cooperative courtship displays to understand these mechanisms. In this species, the cooperative display is modulated by testosterone, which promotes cooperation in non-territorial birds, but suppresses cooperation in territory holders. We sought to understand the neurogenomic underpinnings of three related traits: social status, cooperative display behaviour and testosterone phenotype. To do this, we profiled gene expression in 10 brain nuclei spanning the social decision-making network (SDMN), and two key endocrine tissues that regulate social behaviour. We associated gene expression with each bird's behavioural and endocrine profile derived from 3 years of repeated measures taken from free-living birds in the Ecuadorian Amazon. We found distinct landscapes of constitutive gene expression were associated with social status, testosterone phenotype and cooperation, reflecting the modular organization and engagement of neuroendocrine tissues. Sex-steroid and neuropeptide signalling appeared to be important in mediating status-specific relationships between testosterone and cooperation, suggesting shared regulatory mechanisms with male aggressive and sexual behaviours. We also identified differentially regulated genes involved in cellular activity and synaptic potentiation, suggesting multiple mechanisms underpin these genomic states. Finally, we identified SDMN-wide gene expression differences between territorial and floater males that could form the basis of 'status-specific' neurophysiological phenotypes, potentially mediated by testosterone and growth hormone. Overall, our findings provide new, systems-level insights into the mechanisms of cooperative behaviour and suggest that differences in neurogenomic state are the basis for individual differences in social behaviour.

Evolution of the Growth Hormone Gene Duplication in Passerine Birds.

Birds of the order Passeriformes represent the most speciose order of land vertebrates. Despite strong scientific interest in this super-radiation, genetic traits unique to passerines are not well characterized. A duplicate copy of growth hormone (GH) is the only gene known to be present in all major lineages of passerines, but not in other birds. GH genes plausibly influence extreme life history traits that passerines exhibit, including the shortest embryo-to-fledging developmental period of any avian order. To unravel the implications of this GH duplication, we investigated the molecular evolution of the ancestral avian GH gene (GH or GH1) and the novel passerine GH paralog (GH2), using 497 gene sequences extracted from 342 genomes. Passerine GH1 and GH2 are reciprocally monophyletic, consistent with a single duplication event from a microchromosome onto a macrochromosome in a common ancestor of extant passerines. Additional chromosomal rearrangements have changed the syntenic and potential regulatory context of these genes. Both passerine GH1 and GH2 display substantially higher rates of nonsynonymous codon change than non-passerine avian GH, suggesting positive selection following duplication. A site involved in signal peptide cleavage is under selection in both paralogs. Other sites under positive selection differ between the two paralogs, but many are clustered in one region of a 3D model of the protein. Both paralogs retain key functional features and are actively but differentially expressed in two major passerine suborders. These phenomena suggest that GH genes may be evolving novel adaptive roles in passerine birds.

Sperm Storage in a Family-Living Lizard, the Tree Skink (Egernia striolata).

The ability to produce viable offspring without recently mating, either through sperm storage or parthenogenesis, can provide fitness advantages under a suite of challenging ecological scenarios. Using genetic analysis, we demonstrate that 3 wild-caught female Tree Skinks (Egernia striolata) reproduced in captivity with no access to males for over a year, and that this is best explained by sperm storage. To the best of our knowledge, this is the first time female sperm storage has been documented in any monogamous family-living reptile, including social Australian egerniine skinks (from the subfamily Egerniinae). Furthermore, by using paternal reconstruction of genotypes we show that captive-born offspring produced by the same females in the preceding year, presumably without sperm storage, were sired by different males. We qualitatively compared aspects of these females' mates and offspring between years. The parents of each litter were unrelated, but paternal and offspring genotypes from litters resulting from stored sperm were more heterozygous than those inferred to be from recent matings. Family-living egerniine skinks generally have low rates of multiple paternity, yet our study suggests that female sperm storage, potentially from outside social partners, offers the real possibility of benefits. Possible benefits include increasing genetic compatibility of mates and avoiding inbreeding depression via cryptic female choice. Sperm storage in Tree Skinks, a family-living lizard with a monogamous mating system, suggests that females may bet-hedge through extra-pair copulation with more heterozygous males, reinforcing the idea that females could have more control on reproductive outcomes than previously thought.

Behavioral Genetics: Dissecting a Supergene to Understand Behavior.

New research shows how alternative 'supergene' alleles of Estrogen Receptor 1 are differentially expressed in specific brain nuclei causing aggressive behavior in the white-throated sparrow.

Three Molecular Markers Show No Evidence of Population Genetic Structure in the Gouldian Finch (Erythrura gouldiae).

Assessment of genetic diversity and connectivity between regions can inform conservation managers about risk of inbreeding, potential for adaptation and where population boundaries lie. The Gouldian finch (Erythrura gouldiae) is a threatened species in northern Australia, occupying the savannah woodlands of the biogeographically complex monsoon tropics. We present the most comprehensive population genetic analysis of diversity and structure the Gouldian finch using 16 microsatellite markers, mitochondrial control region and 3,389 SNPs from genotyping-by-sequencing. Mitochondrial diversity is compared across three related, co-distributed finches with different conservation threat-statuses. There was no evidence of genetic differentiation across the western part of the range in any of the molecular markers, and haplotype diversity but not richness was lower than a common co-distributed species. Individuals within the panmictic population in the west may be highly dispersive within this wide area, and we urge caution when interpreting anecdotal observations of changes to the distribution and/or flock sizes of Gouldian finch populations as evidence of overall changes to the population size of this species.

Colour polymorphism is likely to be disadvantageous to some populations and species due to genetic architecture and morph interactions.

Polymorphism describes two or more distinct, genetically determined, phenotypes that co-occur in the same population, where the rarest morph is maintained at a frequency above the mutation rate (Ford 1945; Huxley 1955). In a recent opinion piece, we explored a new idea regarding the role of genetic architectures and morph interactions in colour polymorphisms and how this can negatively affect population performance (Bolton et al. 2015). In this issue of Molecular Ecology, Forsman (2016) thoroughly discusses the current evidence for polymorphisms enhancing population performance and critiques the validity of the definitions of polymorphism we use in our original paper. We respond by clarifying that the negative consequences of polymorphisms that we discussed are likely to be most pertinent in species that have a particular set of characteristics, such as strong sexual or social interactions between morphs and discrete genetic architectures. Although it was not our intention to redefine polymorphism, we do believe that there should be further discussion about refining or characterizing balanced polymorphisms with respect to the degree of morph sympatry, discreteness of traits and their underlying genetic architecture, and the types of selection that drive and maintain the variation. The latter describes whether polymorphism is primarily maintained by external factors such as predation pressure or internal factors such as interactions with members of the same species. The contribution of Forsman (2016) is useful to this discussion, and we hope that our exchange of opinions will inspire new empirical and theoretical ideas on the origin and maintenance of colour polymorphisms.

The danger within: the role of genetic, behavioural and ecological factors in population persistence of colour polymorphic species.

Polymorphic species have been the focus of important work in evolutionary biology. It has been suggested that colour polymorphic species have specific evolutionary and population dynamics that enable them to persist through environmental changes better than less variable species. We suggest that recent empirical and theoretical work indicates that polymorphic species may be more vulnerable to extinction than previously thought. This vulnerability arises because these species often have a number of correlated sexual, behavioural, life history and ecological traits, which can have a simple genetic underpinning. When exacerbated by environmental change, these alternate strategies can lead to conflict between morphs at the genomic and population levels, which can directly or indirectly affect population and evolutionary dynamics. In this perspective, we identify a number of ways in which the nature of the correlated traits, their underpinning genetic architecture, and the inevitable interactions between colour morphs can result in a reduction in population fitness. The principles illustrated here apply to all kinds of discrete polymorphism (e.g. behavioural syndromes), but we focus primarily on colour polymorphism because they are well studied. We urge further empirical investigation of the genetic architecture and interactions in polymorphic species to elucidate the impact on population fitness.