Evolutionary history, genomic adaptation to toxic diet and extinction of the Carolina parakeet

As the only endemic Neotropical parrot to have recently lived in the northern hemisphere, the Carolina parakeet (Conuropsis carolinensis) was an iconic North American bird. The last surviving specimen died in the Cincinnati Zoo in 1918 (Elphick et al., 2010). The cause of its extinction remains contentious: besides excessive mortality associated to habitat destruction and active hunting, their survival could have been negatively affected by its range having become increasingly patchy (Burgio et al., 2017), or by the exposure to poultry pathogens (Snyder, 2004; Snyder and Russel, 2002). In addition, the Carolina parakeet showed a predilection for cockleburs, an herbaceous plant that contains a powerful toxin, carboxyatractyloside, or CAT (Stuart et al., 1981), which did not seem to affect them but made the birds notoriously toxic to most predators (Snyder, 2004). To explore the demographic history of this bird we generated the complete genomic sequence of a preserved specimen held in a private collection in Spain, as well as of a close extant relative, Aratinga solstitialis. We identified two non-synonymous genetic changes in two highly conserved proteins known to interact with CAT that could underlie a specific dietary adaptation to this toxin. Our genomic analyses did not reveal evidence of a dramatic past demographic decline in the Carolina parakeet; also, its genome did not exhibit the long runs of homozygosity that are signals of recent inbreeding and are typically found in endangered species. As such, our results suggest its extinction was an abrupt process, and thus likely solely attributable to human causes.

作为目前已知唯一曾栖息于北半球的特有新热带鹦鹉，卡罗莱纳长尾鹦鹉（Conuropsis carolinensis）是极具代表性的北美鸟类。最后一只存活个体于1918年在辛辛那提动物园（Cincinnati Zoo）离世（Elphick等，2010）。其灭绝原因至今尚存争议：除栖息地破坏与过度捕猎导致的过高死亡率外，分布范围日益破碎化（Burgio等，2017）或接触家禽病原体（Snyder，2004；Snyder与Russel，2002）均可能对其生存造成负面影响。此外，卡罗莱纳长尾鹦鹉偏好取食苍耳——一种含有强效毒素羧基苍术苷（carboxyatractyloside，简称CAT）的草本植物（Stuart等，1981）；该毒素对鹦鹉本身无明显影响，却使其对绝大多数捕食者具备致命毒性，这一特性广为人知。为探究该物种的种群历史，我们对西班牙私人馆藏的一具保存标本，以及近缘现生物种太阳锥尾鹦鹉（Aratinga solstitialis）的完整基因组序列进行了测定。我们在两种已知可与CAT结合的高度保守蛋白中，发现了两处非同义遗传变异，这或为该物种针对该毒素形成特异性饮食适应性的分子基础。基因组分析未发现卡罗莱纳长尾鹦鹉曾经历剧烈种群衰退的证据；同时，其基因组也未出现濒危物种常见的、作为近期近交信号的长纯合子区域。据此，本研究结果表明，卡罗莱纳长尾鹦鹉的灭绝是一个突发过程，因此其灭绝原因或可完全归咎于人类活动。