Data from: Evidence of the phenotypic expression of a lethal recessive allele under inbreeding in a wild population of conservation concern

Deleterious recessive alleles that are masked in outbred populations are predicted to be expressed in small, inbred populations, reducing both individual fitness and population viability. However, there are few definitive examples of phenotypic expression of lethal recessive alleles under inbreeding conditions in wild populations. Studies that demonstrate the action of such alleles, and infer their distribution and dynamics, are required to understand their potential impact on population viability and inform management responses. The Scottish population of red-billed choughs (Pyrrhocorax pyrrhocorax), which currently totals <60 breeding pairs and is of major conservation concern, has recently been affected by lethal blindness in nestlings. We used family data to show that the pattern of occurrence of blindness within and across affected families that produced blind nestlings was exactly 0·25, matching that expected given a single-locus autosomal lethal recessive allele. Furthermore, the observed distribution of blind nestlings within affected families did not differ from that expected given Mendelian inheritance of such an allele. Relatedness estimates showed that individuals from affected families were not more closely related to each other than they were to individuals from unaffected families that did not produce blind nestlings. Blind individuals tended to be less heterozygous than non-blind individuals, as expected if blindness was caused by the expression of a recessive allele under inbreeding. However, there was no difference in the variance in heterozygosity estimates, suggesting that some blind individuals were relatively outbred. These results suggest carriers of the blindness allele may be widely distributed across contemporary families rather than restricted to a single family lineage, implying that the allele has persisted across multiple generations. Blindness occurred at low frequency (affecting 1·6% of observed nestlings since 1981). However, affected families had larger initial brood sizes than unaffected families. Such high fecundity of carriers of a lethal recessive allele might reflect overdominance, potentially reducing purging and increasing allele persistence probability. We thereby demonstrate the phenotypic expression of a lethal recessive allele in a wild population of conservation concern, and provide a general framework for inferring allele distribution and persistence and informing management responses.

在远交种群（outbred populations）中被掩盖的有害隐性等位基因（deleterious recessive alleles），预计会在小型近交种群（inbred populations）中得以表达，进而降低个体适合度（individual fitness）与种群生存力（population viability）。然而，野生种群近交条件下致死隐性等位基因（lethal recessive allele）的表型表达案例仍较为匮乏。目前亟需开展能够证实这类等位基因作用、并推断其分布与动态的研究，以阐明其对种群生存力的潜在影响，并为保护管理对策提供科学依据。苏格兰红嘴山鸦（red-billed choughs，学名Pyrrhocorax pyrrhocorax）种群当前仅存不足60对繁殖个体，属于受重点关注的保护对象，近期出现了雏鸟致死性失明病例。我们借助家系数据分析发现，在产生失明雏鸟的受影响家系内部及家系间，失明症状的发生比例恰好为0.25，这与单基因常染色体致死隐性等位基因（single-locus autosomal lethal recessive allele）的预期模式完全吻合。此外，受影响家系内失明雏鸟的分布情况，也符合该类等位基因孟德尔遗传（Mendelian inheritance）的预期结果。亲缘关系估计结果表明，受影响家系内个体间的亲缘亲密程度，与未产生失明雏鸟的未受影响家系个体间并无显著差异。与非失明个体相比，失明个体的杂合度（heterozygosity）普遍更低，这符合近交条件下隐性等位基因表达导致失明的预期。然而，杂合度估计值的方差并无显著差异，这提示部分失明个体的近交程度相对较低。上述结果表明，失明等位基因的携带者可能广泛分布于当代各个家系中，而非局限于单一家庭谱系，这意味着该等位基因已在种群中存续了多代。失明症状的发生频率较低（1981年以来的观测雏鸟中受影响比例为1.6%）。不过，受影响家系的初始窝卵数要大于未受影响家系。致死隐性等位基因携带者的这种高繁殖力，可能反映了超显性（overdominance）效应，进而减缓了等位基因清除（purging）过程，提升了该等位基因的存续概率。本研究证实了受保护关注的野生种群中致死隐性等位基因的表型表达，并为推断等位基因的分布与存续模式、制定针对性管理对策提供了通用分析框架。