Disturbance-mediated hybridization in black-capped and mountain chickadees

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, black-capped, and mountain chickadees,
using both genomic and citizen science datasets. First, we genotyped 409
individuals from across both species’ ranges using reduced-representation
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 significantly increased with habitat disturbance, 2)
more hybrids were sampled in disturbed habitats, 3) mean hybrid indexes
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.

人类栖息地干扰可推动亲缘关系相近、但通常存在生殖隔离的物种间发生杂交。本研究结合基因组学与公民科学数据集，探究了人类栖息地干扰是否与两种亲缘关系相近的鸣禽——黑顶山雀（black-capped chickadee）与山地山雀（mountain chickadee）——间的杂交存在关联。首先，我们利用简化基因组测序（reduced-representation genome sequencing）技术，对两种鸟类分布范围内的409个个体进行了基因分型，并将遗传渐渗（genetic admixture）指标与人类景观干扰的综合度量值进行了对比分析。随后，我们借助eBird观测数据，将观测到经表型鉴定的杂合体的位点的人类景观干扰值，与仅观测到任一亲本物种的位点进行对比，以明确山雀杂合体是否更多被记录于受干扰程度更高的区域。研究结果显示，黑顶山雀与山地山雀间的杂交事件与人类栖息地干扰呈显著正相关。基于基因组数据，我们得到如下结论：1）杂合指数（hybrid index）随栖息地干扰程度升高而显著上升；2）受干扰生境中采样到的杂合体数量更多；3）受干扰生境的平均杂合指数显著高于野生生境；4）相较于亲本物种，杂合体所在生境的干扰值显著更高。借助eBird数据，我们发现杂合体与黑顶山雀均比山地山雀更显著地倾向于栖息在受干扰生境中。令人意外的是，我们采样的黑顶山雀几乎均携带一定比例的杂合祖先血统，而仅检测到极少量山地山雀回交（backcross）个体。本研究结果表明，黑顶山雀与山地山雀间的杂交现象广泛存在，但初始杂交事件（即F1个体）较为罕见——仅检测到极少量F1个体。我们由此得出结论：人类栖息地干扰会削弱山雀种群间的合子前生殖隔离（pre-zygotic reproductive barrier），且合子后生殖隔离（post-zygotic isolation）并不完全。在全球环境快速变化的当下，探究大规模栖息地干扰后新近发生杂交的物种的演化命运，是成功保护遗传生物多样性的一项全新且紧迫的课题。