An official website of the United States government
Abstract Early lineage diversification is central to understand what mutational events drive species divergence. Particularly, gene misregulation in interspecific hybrids can inform about what genes and pathways underlie hybrid dysfunction. InDrosophilahybrids, how regulatory evolution impacts different reproductive tissues remains understudied. Here, we generate a new genome assembly and annotation inDrosophila willistoniand analyse the patterns of transcriptome divergence between two allopatrically evolvedD. willistonisubspecies, their male sterile and female fertile hybrid progeny across testis, male accessory gland, and ovary. Patterns of transcriptome divergence and modes of regulatory evolution were tissue‐specific. Despite no indication for cell‐type differences in hybrid testis, this tissue exhibited the largest magnitude of expression differentiation between subspecies and between parentals and hybrids. No evidence for anomalous dosage compensation in hybrid male tissues was detected nor was a differential role for the neo‐ and the ancestral arms of theD. willistoni Xchromosome. Compared to the autosomes, theXchromosome appeared enriched for transgressively expressed genes in testis despite being the least differentiated in expression between subspecies. Evidence for fine genome clustering of transgressively expressed genes suggests a role of chromatin structure on hybrid gene misregulation. Lastly, transgressively expressed genes in the testis of the sterile male progeny were enriched for GO terms not typically associated with sperm function, instead hinting at anomalous development of the reproductive tissue. Our thorough tissue‐level portrait of transcriptome differentiation between recently divergedD. willistonisubspecies and their hybrids provides a more nuanced view of early regulatory changes during speciation.
more »
« less
Gene regulation and speciation in a migratory divide between songbirds
Abstract Behavioral variation abounds in nature. This variation is important for adaptation and speciation, but its molecular basis remains elusive. Here, we use a hybrid zone between two subspecies of songbirds that differ in migration – an ecologically important and taxonomically widespread behavior---to gain insight into this topic. We measure gene expression in five brain regions. Differential expression between migratory states was dominated by circadian genes in all brain regions. The remaining patterns were largely brain-region specific. For example, expression differences between the subspecies that interact with migratory state likely help maintain reproductive isolation in this system and were documented in only three brain regions. Contrary to existing work on regulatory mechanisms underlying species-specific traits, two lines of evidence suggest that trans- (vs. cis) regulatory changes underlie these patterns – no evidence for allele-specific expression in hybrids and minimal associations between genomic differentiation and expression differences. Additional work with hybrids shows expression levels were often distinct (transgressive) from parental forms. Behavioral contrasts and functional enrichment analyses allowed us to connect these patterns to mitonuclear incompatibilities and compensatory responses to stress that could exacerbate selection on hybrids and contribute to speciation.
more »
« less
- Award ID(s):
- 2143004
- PAR ID:
- 10483825
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 15
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Extrinsic postzygotic isolation, where hybrids experience reductions in fitness due to a mismatch with their environment, is central to speciation. Knowledge of genetic variants that underlie extrinsic isolation is crucial for understanding the early stages of speciation. Differences in seasonal migration are strong candidates for extrinsic isolation (e.g., if hybrids take intermediate and inferior routes compared to pure forms). Here, we used a hybrid zone between two subspecies of the songbird Swainson’s thrush (Catharus ustulatus) with different migratory routes and tests for viability selection (locus-specific changes in interspecific heterozygosity and ancestry mismatch across age classes) to gain insight into the genetic basis of extrinsic isolation. Using data from over 900 individuals we find strong evidence for viability selection on both interspecific heterozygosity and ancestry mismatch at loci linked to migration. Much of this selection was dependent on genome-wide ancestry; as expected, a subset of hybrids exhibited reduced viability, but remarkably, another subset appears to fill an unoccupied fitness peak within the species, exhibiting higher viability than even parental forms. Many of the variants that influence hybrid viability appear to occur in structural variants, including a putative pericentric inversion. Our study emphasizes the importance of epistatic interactions and structural variants in speciation.more » « less
-
Abstract Divergent adaptation can promote ecological speciation if hybrids have reduced fitness because they are poorly adapted to either parental niche. We tested for ecologically dependent, postzygotic isolation between two subspecies of Swainson’s thrushes, which form a migratory divide and hybrid zone in western North America. To do this, we translocated backcrossed and admixed birds from the hybrid zone into the range of each subspecies in the beginning of fall migration. We estimated a proxy for their survival on migration and migratory behaviour using automated radio tracking. Apparent survival of birds in the two environments did not depend on their genomic ancestry, suggesting that Swainson’s thrushes’ divergent adaptation to different fall migration routes does not fit the classic model of ecological speciation. We propose an alternate scenario where ecological selection on migration may interact with intrinsic maladaptation in hybrids to cause hybrid survival on migration. By translocating birds from the same genomic backgrounds into different environments, our experiment also allowed us to distinguish between the effects of environmental relative to genetic contributors to their migratory behaviour. We found evidence that both genetic and environmental factors influence migratory behaviour, as an effect of genomic ancestry on initial migratory trajectories depended on the start location for migration but birds ultimately followed expected routes given their genomic ancestries.more » « less
-
Abstract Although the endocrine system likely plays an important role in orchestrating the transition to a migratory state, the specific mechanisms by which this occurs remain poorly understood. Changes in glucocorticoid signaling are one proposed mechanism that may be important in migratory transitions. Although previous work has focused on the role of changes in circulating glucocorticoids, another potential mechanism is changes in the expression of its cognate receptors. Here, we test this hypothesis by comparing mRNA expression of the genes for the mineralocorticoid receptor ( MR ) and glucocorticoid receptor ( GR ) in two brain regions implicated in the regulation of migratory behavior (the hippocampus and hypothalamus) in pine siskins ( Spinus pinus ) sampled before or after the transition to a spring nomadic migratory state. Compared to pre-migratory birds, migratory birds had body conditions more indicative of physiological preparations for migration (e.g., larger body mass), and greater levels of nocturnal migratory restlessness. However, we found no differences between pre-migratory and migratory birds in the expression of GR or MR mRNA in either the hippocampus or hypothalamus. Thus, differences in expression of receptors for glucocorticoids do not appear to underly the observed differences in physiology and behavior across a migratory transition. Taken together with previous results showing no change in circulating corticosterone levels during this transition, our findings provide no evidence for a role of glucocorticoid signaling in the spring migratory transition of this species.more » « less
-
Abstract Migratory divides, hybrid zones between populations that use different seasonal migration routes, are hypothesised to contribute to speciation. Specifically, relative to parental species, hybrids at divides are predicted to exhibit (1) intermediate migratory behaviour and (2) reduced fitness as a result. We provide the first direct test of the second prediction here with one of the largest existing avian tracking datasets, leveraging a divide between Swainson's thrushes where the first prediction is supported. Using detection rates as a proxy for survival, our results supported the migratory divide hypothesis with lower survival rates for hybrids than parental forms. This finding was juvenile‐specific (vs. adults), suggesting selection against hybrids is stronger earlier in life. Reduced hybrid survival was not explained by selection against intermediate phenotypes or negative interactions among phenotypes. Additional work connecting specific features of migration is needed, but these patterns provide strong support for migration as an ecological driver of speciation.more » « less
