Biology subjects

Enbody, E. D.

Publications and source records attributed to Enbody, E. D..

9 recordsLinked to original sources

bioRxiv2026

Sex and breeding stage differences in neurogenomic profiles reflect hormone signaling in a socially polyandrous shorebird

In sex-role reversed species, females are socially polyandrous and compete for multiple mates, whereas males conduct the majority of parental care. To understand the extent to which physiological differences between females and males are shaped by sex roles, we examined sex differences in gene expression in sex-role reversed northern jacanas (Jacana spinosa). Given that females compete for mating opportunities, and males cycle between courtship and parental care, we predicted that transcriptomic profiles would be more similar between females and courting males, in contrast to female and parenting males. Leveraging a high quality de novo genome assembly, we conducted RNA-seq on two brain regions associated with the regulation of social behavior: the preoptic area of the hypothalamus and the nucleus taeniae. The majority of genes differentially expressed between the sexes were male-biased. Of these male-biased genes, the majority were located on the Z-chromosome. Contrary to our prediction, the greatest difference in autosomal gene expression was between females and courting males, in the preoptic area of the hypothalamus. Several differentially expressed genes related to elements of hormone signaling that are likely to be behaviorally salient, including higher expression of androgen receptor in females relative to parenting males, and higher expression of prolactin receptor in males, regardless of breeding stage. Some sex-associated gene networks were also associated with competitive traits, whereas others were associated with aggressive behaviors, regardless of sex. Few genes were differentially expressed between courting and parenting males, yet some nonetheless had connections to behavioral endocrinology, including prolactin, thyroid and insulin-like growth factor pathways. Our investigation of sex differences in gene expression can help to reveal the molecular mechanisms underlying female competition and male parental care in socially polyandrous species. We conclude that social polyandry is not a simple reversal in the direction of sex-biased gene expression in the brain, but rather a result of complex genetic and hormonal interactions that warrants further study.

genomics↗

bioRxiv2023

Copy number variation and elevated genetic diversity at immune trait loci in Atlantic and Pacific herring

Atlantic and Pacific herring are sister species that diverged about 2 million years ago. Here we describe a genome comparison of the two species that reveal high genome-wide differentiation as expected for two distinct species but with islands of remarkably low genetic differentiation as measured by an FST analysis. However, this is not caused by low interspecies sequence divergence but an exceptionally high estimated intraspecies nucleotide diversity. These high diversity regions are not enriched for repeats but are highly enriched for immune trait-related genes. This enrichment includes classical immunity genes, such as immunoglobulin, T-cell receptor and major histocompatibility complex genes, but also a substantial number of genes with a role in the innate immune system. An analysis of long-read based assemblies from two Atlantic herring individuals revealed extensive copy number variation at these genomic regions, indicating that the elevated intraspecies nucleotide diversities was partially due to the cross-mapping of short reads. This study demonstrates that copy number expansion and variation is a characteristic feature of immune trait loci in herring and that this genetic diversity is likely to contribute to resistance to infectious diseases in extremely abundant species, such as the Atlantic and Pacific herring. Another important implication is that these loci are blind spots in classical genome-wide screens for genetic differentiation using short-read data, not only in herring, likely also in other species harboring qualitatively similar variation at immune trait loci. SignificanceThis study has revealed an extensive copy number variation and high nucleotide diversity at genes related to the immune system in Atlantic herring. Our analysis of previously published data in teleost species indicate that this is probably a widespread pattern among vertebrates. We also document that population genetic parameters estimated using short-read sequencing data are unreliable for these regions due to their complexity. They will also appear as blind spots in genome scans for regions of genetic differentiation based on FST statistics due to the very high within population nucleotide diversity. We show how long-read data can be used to decipher the gene organization and genetic diversity at these regions.

genomics↗

bioRxiv2023

Introgression underlies phylogenetic uncertainty but not parallel plumage evolution in a recent songbird radiation

Instances of parallel phenotypic evolution offer great opportunities to understand the evolutionary processes underlying phenotypic changes. However, confirming parallel phenotypic evolution and studying its causes requires a robust phylogenetic framework. One such example is the "black-and-white wagtails", a group of five species in the songbird genus Motacilla: one species, the White Wagtail (M. alba), shows wide intra-specific plumage variation, while the four others form two pairs of very similar-looking species (African Pied Wagtail M. aguimp + Mekong Wagtail M. samveasnae and Japanese Wagtail M. grandis + White-browed Wagtail M. maderaspatensis, respectively). However, the two species in each of these pairs were not recovered as sisters in previous phylogenetic inferences. Their relationships varied depending on the markers used, suggesting that gene tree heterogeneity might have hampered accurate phylogenetic inference. Here, we use whole genome resequencing data to explore the phylogenetic relationships within this group, with a special emphasis on characterizing the extent of gene tree heterogeneity and its underlying causes. We first used multispecies coalescent methods to generate a "complete evidence" phylogenetic hypothesis based on genome-wide variants, while accounting for incomplete lineage sorting and introgression. We then investigated the variation in phylogenetic signal across the genome, to quantify the extent of discordance across genomic regions, and test its underlying causes. We found that wagtail genomes are mosaics of regions supporting variable genealogies, because of ILS and inter-specific introgression. The most common topology across the genome, supporting M. alba and M. aguimp as sister species, appears to be influenced by ancient introgression. Additionally, we inferred another ancient introgression event, between M. alba and M. grandis. By combining results from multiple analyses, we propose a phylogenetic network for the black-and-white wagtails that confirms that similar phenotypes evolved in non-sister lineages, supporting parallel plumage evolution. Furthermore, the inferred reticulations do not connect species with similar plumage coloration, suggesting that introgression does not underlie parallel plumage evolution in this group. Our results demonstrate the importance of investigation of genome-wide patterns of gene tree heterogeneity to help understanding the mechanisms underlying phenotypic evolution.

evolutionary biology↗

bioRxiv2023

Does capacity to elevate androgens underlie variation in female ornamentation and territoriality in White-shouldered Fairywren (Malurus alboscapulatus)?

Historic bias toward study of male sex hormones and sexual signals currently constrains our perspective of hormone--behavior--phenotype relationships. Resolving how ornamented female phenotypes evolve is particularly important for understanding the diversity of social signals across taxa. Studies of both males and females in taxa with variable female phenotypes are needed to establish whether sexes share mechanisms underlying expression of signaling phenotypes and behavior. White-shouldered Fairywren (Malurus alboscapulatus) subspecies vary in female ornamentation, baseline circulating androgens, and response to territorial intrusion. The moretoni ornamented female subspecies show higher female, but lower male androgens, and a stronger pair territorial response relative to pairs from the lorentzi unornamented female subspecies. Here we address whether subspecific differences in female ornamentation, baseline androgens, and pair territoriality are associated with ability to elevate androgens following gonadotropin releasing hormone (GnRH) challenge and in response to simulated territorial intrusion. We find that subspecies do not differ in their capacity to circulate androgens in either sex following GnRH or territorial intrusion challenges. Whereas pre-GnRH androgens were somewhat predictive of degree of response to territorial intrusions, higher androgens were associated with lower territorial aggression. Post-GnRH androgens were not predictive of response to simulated intruders, nor did females sampled during intrusion elevate androgens relative to flushed controls, suggesting that increased androgens are not necessary for the expression of territorial defense behaviors. Collectively, our results suggest that capacity to produce and circulate androgens does not underlie subspecific patterns of female ornamentation, territoriality, and baseline androgens.

animal behavior and cognition↗

bioRxiv2022

Large effect loci have a prominent role in Darwin's finch evolution

A fundamental goal in evolutionary biology is to understand the genetic architecture of adaptive traits and its evolutionary relevance. Using whole-genome data of 3,958 Darwins finches on the Galapagos Island of Daphne Major we identify six loci of large effect that explain 46% of the variation in beak size of Geospiza fortis, a key ecological trait. Allele frequency changes across 30 years at these loci affected beak morphology in two ways. An abrupt change in beak size occurred in Geospiza fortis as a result of natural selection associated with a drought, and a more gradual change occurred in G. scandens as a result of introgressive hybridization. This study demonstrates how large effect loci are a major contributor to the genetic architecture of rapid diversification during adaptive radiations. One Sentence SummaryAllele frequency change at six loci of large effect causes evolutionary change in key ecological traits.

evolutionary biology↗

bioRxiv2021

Male White-shouldered Fairywrens (Malurus alboscapulatus) elevate testosterone when courting females but not during territorial challenges

Testosterone mediates suites of physical and behavioral traits across vertebrates, and circulation varies considerably across and within taxa. However, an understanding of the causal factors of variation in circulating testosterone has proven difficult despite decades of research. According to the challenge hypothesis, agonistic interactions between males immediately prior to the breeding season produce the highest levels of testosterone measured during this period. While many studies have provided support for this hypothesis, most species do not respond to male-male competition by elevating testosterone. As a result, a recent revision of the hypothesis ( challenge hypothesis 2.0) places male-female interactions as the primary cause of rapid elevations in testosterone circulation in male vertebrates. Here, we offer a test of both iterations of the challenge hypothesis in a tropical bird species. We first illustrate that male White-shouldered Fairywrens (Malurus alboscapulatus) differ by subspecies in plasma testosterone concentrations. Then we use a social network approach to find that males of the subspecies with higher testosterone are characterized by greater social interaction scores, including more time aggregating to perform sexual displays. Next, we use a controlled experiment to test whether males respond to simulated territorial intrusion or courtship interaction contexts by elevating testosterone. Males sampled during courtship had greater plasma testosterone both relative to flushed controls and males sampled during simulated intrusion. Ultimately, our results are consistent with challenge hypothesis 2.0, as males rapidly elevated testosterone following interactions with females, but not during territorial challenges.

animal behavior and cognition↗

bioRxiv2021

Darwin's finches - an adaptive radiation constructed from ancestral genetic modules

Recent adaptive radiations are models for investigating mechanisms contributing to the evolution of biodiversity. An unresolved question is the relative importance of new mutations, ancestral variants, and introgressive hybridization for phenotypic evolution and speciation. Here we address this issue using Darwins finches, which vary in size from an 8g warbler finch with a pointed beak to a 40g large ground finch with a massive blunt beak. We present a highly contiguous genome assembly for one of the species and investigate the genomic architecture underlying phenotypic diversity in the entire radiation. Admixture mapping for beak and body size in the small, medium and large ground finches revealed 28 loci showing strong genetic differentiation. These loci represent ancestral haplotype blocks with origins as old as the Darwins finch phylogeny (1-2 million years). Genes expressed in the developing beak are overrepresented in these genomic regions. Frequencies of allelic variants at the 28 loci covary with phenotypic similarities in body and beak size across the Darwins finch phylogeny. These ancestral haplotypes constitute genetic modules for selection, and act as key determinants of the exceptional phenotypic diversity of Darwins finches. Such ancestral haplotype blocks can be critical for how species adapt to environmental variability and change.

evolutionary biology↗

bioRxiv2021

Transspecies beak color polymorphism in the Darwin's finch radiation

Carotenoid-based polymorphisms are widespread in populations of birds, fish, and reptiles1, but little is known of how they affect fitness and are maintained as species multiply2. We report a combined field and molecular-genetic investigation of a nestling beak color polymorphism in Darwins finches. Beaks are pink or yellow, and yellow is recessive3. Here we show that the polymorphism arose in the Galapagos approximately half a million years ago through a regulatory mutation in the BCO2 gene, and is shared by 14 descendant species. The frequency of the yellow genotype is associated with cactus flower abundance in cactus finches, and is altered by introgressive hybridization. The polymorphism is most likely a balanced polymorphism, maintained by ecological selection pressures associated with diet, and augmented by occasional interspecific introgression. Polymorphisms that are hidden as adults, as here, may contribute to evolutionary diversification in underappreciated ways in other systems.

evolutionary biology↗

bioRxiv2020

Testosterone induces a female ornament followed by enhanced territoriality in a tropical songbird

We know little of the proximate mechanisms underlying expression of signaling traits in female vertebrates. Across males the expression of sexual and competitive traits, including ornamentation and aggressive behavior, is often mediated by testosterone. In the White-shouldered Fairywren (Malurus alboscapulatus) of New Guinea, females of different subspecies differ in presence or absence of white shoulder patches and melanic plumage, while males are uniformly ornamented. Previous work has shown that ornamented females circulate more testosterone and exhibit more territorial aggression than do unornamented females. We investigated the degree to which testosterone regulates expression of ornamental plumage and territorial behavior by implanting free-living unornamented females with testosterone. Every testosterone-treated female produced a male-like cloacal protuberance, and 15 of 20 replaced plucked brown feathers with white shoulder patch feathers, but did not produce melanic plumage characteristic of ornamented females. Testosterone treatment did not elevate territorial behavior prior to production of the plumage ornament and exhaustion of the implant. However, females with experimentally induced ornamentation, but exhausted implants, increased the vocal components of territory defense relative to fully unornamented control and also to testosterone-implanted females. Our results suggest that testosterone induces partial acquisition of the ornamental plumage phenotype, and that ornament expression, rather than testosterone alone, results in elevated territorial behavior. Lay SummaryTestosterone regulates expression of a suite of competitive traits in male organisms and could have similar function in females. Empirical tests are needed to determine the extent to which testosterone promotes production of ornamentation and competitive behaviors in female animals. We supplemented testosterone in unornamented females of a species where naturally occurring ornamented females circulate higher testosterone and are more territorially aggressive. Implanted females produced partial ornamentation, which was followed by increased territoriality that was apparently unrelated to testosterone circulation itself.

animal behavior and cognition↗