Hybridization between closely related songbirds is related to human habitat disturbance

Abstract

Human habitat disturbances can promote hybridization between closely related, but typically reproductively isolated, species. We explored whether human habitat disturbances are related to hybridization between two closely related songbirds, blackcapped and mountain chickadees, using both genomic and citizen science data sets.First, we genotyped 409 individuals from across both species' ranges using reducedrepresentation genome sequencing and compared measures of genetic admixture to a composite measure of human landscape disturbance. Then, using eBird observations, we compared human landscape disturbance values for sites where phenotypically diagnosed hybrids were observed to locations where either parental species was observed to determine whether hybrid chickadees are reported in more disturbed areas. We found that hybridization between black-capped and mountain chickadees positively correlates with human habitat disturbances. From genomic data, we found that (1) hybrid index (HI) significantly increased with habitat disturbance, (2) more hybrids were sampled in disturbed habitats, (3) mean HIs were higher in disturbed habitats versus wild habitats, and (4) hybrids were detected in habitats with significantly higher disturbance values than parentals. Using eBird data, we found that both hybrid and black-capped chickadees were significantly more disturbance-associated than mountain chickadees. Surprisingly, we found that nearly every black-capped chickadee we sampled contained some proportion of hybrid ancestry, while we detected very few mountain chickadee backcrosses. Our results highlight that hybridization between black-capped and mountain chickadees is widespread, but initial hybridization is rare (few F1s were detected). We conclude that human habitat disturbances can erode pre-zygotic reproductive barriers between chickadees and that post-zygotic isolation is incomplete. Understanding what becomes of recently hybridizing species following large-scale habitat disturbances is a new, but pressing, consideration for successfully preserving genetic biodiversity in a rapidly changing world.

Diverse data sources and new statistical models offer prospects for improving the predictability of anthropogenic hybridization

“…In their new paper, Grabenstein et al (2022) demonstrate that the rate of hybridization between black capped and mountain chickadees ( Poecile atricapillus and P. gambeli respectively) increases with increasing human disturbance. This is an exciting step forward for studies in anthropogenic hybridization, because in addition to demonstrating variation in hybridization rates across different habitats, Grabenstein et al (2022) propose and test human disturbance as a mechanism leading to this hybridization.…”

“…In their new paper, Grabenstein et al (2022) demonstrate that the rate of hybridization between black capped and mountain chickadees ( Poecile atricapillus and P. gambeli respectively) increases with increasing human disturbance. This is an exciting step forward for studies in anthropogenic hybridization, because in addition to demonstrating variation in hybridization rates across different habitats, Grabenstein et al (2022) propose and test human disturbance as a mechanism leading to this hybridization. An innovative aspect of this study is that they test this pattern using both a smaller dataset of 409 birds at 81 replicate sites (genomic and phenotypic data), and using a community collected data resource (reports from eBird) that reports hybrids using phenotypic data only, but from many more locations.…”

“…Notably, they also used a publicly available index of human disturbance that could be applied to all locations. By looking at rates of chickadee hybridization across the overlapping range, and controlling for sympatry, Grabenstein et al (2022) provide convincing evidence for a causal relationship between human disturbance and chickadee hybridization. Furthermore, by including the eBird data in the analyses, Grabenstein et al (2022) show that the effect of disturbance on chickadee hybridization is likely to be a widespread phenomenon.…”

“…By looking at rates of chickadee hybridization across the overlapping range, and controlling for sympatry, Grabenstein et al (2022) provide convincing evidence for a causal relationship between human disturbance and chickadee hybridization. Furthermore, by including the eBird data in the analyses, Grabenstein et al (2022) show that the effect of disturbance on chickadee hybridization is likely to be a widespread phenomenon. If this relationship holds across variation in reproductive isolation across areas of sympatry between parental species, it is possible that understanding this mechanistic relationship will enable prediction of when reproductive isolation breaks down—a major question in conservation genetics when dealing with hybridization.…”

“…While neither chickadee species is currently threatened, these results are encouraging for managing hybridization in threatened taxa as well. If, as has been done in Grabenstein et al (2022), it is possible to predict the breakdown of reproductive isolation based on environmental factors, then wider conservation policies can be enacted for species of conservation concern, without substantial, costly genomic sampling across ranges.…”