Supergenes on Steroids

At the birth of supergenes, the genomic landscape is dramatically re-organized leading to pronounced differences in phenotypes and increased intrasexual diversity. Two of the best-studied supergenes in vertebrates are arguably the inversion polymorphisms on chromosomes 2 and 11 in the white-throated sparrow (Zonotrichia albicollis) and the ruff (Calidris pugnax), respectively. In both species, regions of suppressed recombination determine plumage coloration and social behavioral phenotypes. Despite the apparent lack of gene overlap between these two supergenes, in both cases the alternative phenotypes seem to be driven largely by alterations in steroid hormone pathways. Here, we explore the interplay between genomic architecture and steroid-related genes. Due to the highly pleiotropic effects of such genes and their universal involvement in social behavior and genomic architecture, forces favouring their linkage are likely to have substantial effects on the evolution of behavioral phenotypes, individual fitness, and life history strategies. We propose that the differentiation of steroid-related genes, inside both supergenes, lies at the core of phenotypic differentiation in both of these interesting species.

Aminopeptidase-N modulation assists lean mass anabolism during refuelling in the white-throated sparrow

Songbirds meet the extreme metabolic demands of migration by burning both stored fat and protein. However, catabolizing these endogenous tissues for energy leads to organ atrophy, and reductions in gastrointestinal tissue can be as great as 50% of the pre-flight mass. Remarkably, during stopover refuelling birds quickly regain digestive mass and performance. Aminopeptidase-N (APN) is a brush-border enzyme responsible for late-stage protein digestion and may critically assist tissue reconstruction during the stopover, thus compensating for reduced gut size. We hypothesized that birds recovering from a fast would differentially upregulate APN activity relative to disaccharidases to rapidly process and assimilate dietary protein into lean mass. We fasted 23 wild-caught migratory white-throated sparrows ( Zonotrichia albicollis ) for 48 h to mimic mass reductions experienced during migratory flight and measured intestinal APN activity before the fast, immediately after the fast, and during recovery at 24 h and 48 h post-fast. Total fat mass, lean mass and basal metabolic rate were measured daily. We show that fasted birds maintain APN activity through the fast, despite a 30% reduction in intestine mass, but during refuelling, APN activity increases nearly twofold over pre-fasted individuals. This suggests that dynamically regulating APN may be necessary for rapid protein reconstruction during the stopover.

Genome-wide variation in DNA methylation linked to developmental stage and chromosomal suppression of recombination in white-throated sparrows

ABSTRACTDNA methylation is known to play critical roles in key biological processes. Most of our knowledge on regulatory impacts of DNA methylation has come from laboratory-bred model organisms, which may not exhibit the full extent of variation found in wild populations. Here, we investigated naturally-occurring variation in DNA methylation in a wild avian species, the white-throated sparrow (Zonotrichia albicollis). This species offers exceptional opportunities for studying the link between genetic differentiation and phenotypic traits because of a non-recombining chromosome pair linked to both plumage and behavioral phenotypes. Using novel single-nucleotide resolution methylation maps and gene expression data, we show that DNA methylation and the expression of DNA methyltransferases are significantly higher in adults than in nestlings. Genes for which DNA methylation varied between nestlings and adults were implicated in development and cell differentiation and were located throughout the genome. In contrast, differential methylation between plumage morphs was localized to the non-recombining chromosome pair. One subset of CpGs on the non-recombining chromosome was extremely hypomethylated and localized to transposable elements. Changes in methylation predicted changes in gene expression for both chromosomes. In summary, we demonstrate changes in genome-wide DNA methylation that are associated with development and with specific functional categories of genes in white-throated sparrows. Moreover, we observe substantial DNA methylation reprogramming associated with the suppression of recombination, with implications for genome integrity and gene expression divergence. These results offer an unprecedented view of ongoing epigenetic reprogramming in a wild population.

Vasoactive intestinal peptide as a mediator of the effects of a supergene on social behaviour

Supergenes, or linked groups of alleles that are inherited together, present excellent opportunities to understand gene–behaviour relationships. In white-throated sparrows ( Zonotrichia albicollis ), a supergene on the second chromosome associates with a more aggressive and less parental phenotype. This supergene includes the gene for vasoactive intestinal peptide (VIP), a neuropeptide known to play a causal role in both aggression and parental behaviour. Here, using a free-living population, we compared the levels of VIP mRNA between birds with and without the supergene. We focused on the anterior hypothalamus and infundibular region, two brain regions containing VIP neurons known to play a causal role in aggression and parental behaviour, respectively. First, we show that the supergene enhances VIP expression in the anterior hypothalamus and that expression positively predicts vocal aggression independently of genotype in both sexes. Next, we show that the supergene reduces VIP expression in the infundibular region, which suggests reduced secretion of prolactin, a pro-parental hormone. Thus, the patterns of VIP expression in these two regions are consistent with the enhanced aggression and reduced parental behaviour of birds with the supergene allele. Our results illustrate mechanisms by which elements of genomic architecture, such as supergenes, can contribute to the evolution of alternative behavioural phenotypes.

New avian breeding records for Kugluktuk, Nunavut

New breeding records for 10 species of tundra and boreal nesting birds were documented near the community of Kugluktuk (Nunavut, Canada) over the course of the 2015 and 2016 breeding seasons and incidentally in 2017 and 2018. These species include American Wigeon (Mareca americana), Mallard (Anas platyrhynchos), Northern Shoveler (Anas clypeata), Green-winged Teal (Anas carolinensis), Greater Scaup (Aythya marila), Say’s Phoebe (Sayornis saya), Canada Jay (Perisoreus canadensis), Greycheeked Thrush (Catharus minimus), Yellow-rumped Warbler (Setophaga coronata), and Dark-eyed Junco (Junco hyemalis). Previously unpublished breeding evidence for Bald Eagle (Haliaeetus leucocephalus) is also discussed along with suspected breeding of Barn Swallow (Hirundo rustica), Bohemian Waxwing (Bombycilla garrulus), White-throated Sparrow (Zonotrichia albicollis), and Pine Grosbeak (Pinicola enucleator). These records represent the first described breeding occurrences for these species in the Kitikmeot region, or new records for the mainland of Nunavut. A lack of historical ornithological survey effort in this area has likely led to the diversity of these previously unrecorded breeding observations. These results highlight the need to increase geographic coverage of bird surveys in northern Canada to more accurately delineate the northern limit of breeding ranges and suggest that further formal survey effort will undoubtedly lead to additional new breeding records.

Parent and offspring genotypes influence gene expression in early life

Parents can have profound effects on offspring fitness. Little, however, is known about the mechanisms through which parental care variation influences offspring physiology in natural systems. White-throated sparrows Zonotrichia albicollis (WTSPs) exist in two genetic morphs, tan and white, controlled by a large polymorphic supergene. Morphs mate disassortatively, resulting in two pair types: tan male x white female (TxW) pairs, which provide biparental care and white male x tan female (WxT) pairs, which provide female-biased care. To investigate the effects of parental care variation, we performed RNA-seq on WTSP nestlings sampled from nests of both pair types. Pair type had the largest effect on nestling gene expression, with 881 genes differentially expressed (DE) and seven correlated gene co-expression modules. The DE genes and modules up-regulated in nests with female-biased parental care primarily function in metabolism and stress-related pathways resulting from the overrepresentation of stress response and proteolysis genes. These results show that parental genotypes, a proxy for parental care in this system, alter nestling physiology and highlight avenues of further research investigating the ultimate implications of alternative parental care strategies. Nestlings also exhibited morph-specific gene expression, driven by innate immunity genes and co-expression of genes located in the supergene. Remarkably, we identified the same regulatory hub genes in these blood-derived expression networks as were previously identified in WTSP brains (EPM2A, BPNT1, TAF5L). These hub genes were located within the supergene, highlighting the importance of this gene complex in structuring regulatory networks across diverse tissues.