Data from: Hologenomic speciation: synergy between a male-killing bacterium and sex-linkage creates a ‘magic trait’ in a butterfly hybrid zone

Danaus chrysippus (L.) in Africa comprises four substantially isolated semispecies that are migratory and hybridize on a seasonal basis throughout the eastern and central part of the continent. In the hybrid zone (but not elsewhere), the butterfly is commonly host to a male killing endosymbiotic bacterium, Spiroplasma sp., which principally infects one semispecies, Danaus chrysippus chrysippus in Kenya. A W-autosome mutation, inherited strictly matrilinearly, links B and C colour gene loci, which have thus gained sex-linkage in chrysippus. We have monitored variation in sex ratio and genotype at the A and C colour gene loci for two extended periods of 18 months (2004–5) and 12 months (2009–10) in adults reared from wild eggs laid on trap plants in Kasarani, near Nairobi, Kenya. Additionally, in 2009–10, all surviving adult butterflies were screened for Spiroplasma infection. The hybridizing Kasarani population is highly atypical in three respects, and has apparently been so for some 30 years: first, the sex ratio is permanently female-biased (as expected), although subject to seasonal fluctuation, being lowest (male/female) when D. c. chrysippus (cc) peaks and highest when Danaus chrysippus dorippus (CC) predominates; second, the population is invariably dominated by Cc heterozygotes of both sexes but especially females; and third, cc males are always scarce because they are systematically eliminated by male killing, whereas the CC genotype is male-biased. It is this imbalance of sex versus genotype that determines the massive departure from Hardy–Weinberg equilibrium in the population, in part because cc females have little choice but to pair with C- males. We suggest that: first, Cc hybrids of both sexes fail to disperse in the company of either parental semispecies; second, Spiroplasma positive females carrying the W-autosome mutation have a selective advantage over females that lack the translocation; third, the endoparasite and the translocation create a ‘magic trait’ linkage group that underlies hologenomic reproductive isolation between two emerging species, D. c. chrysippus and D. c. dorippus; and, fourth, that the predominance of males in dorippus suggests that individuals must be protected by a male-killing suppressor gene. By contrast to the C locus, Aa heterozygotes are in substantial and permanent deficit, suggesting either assortative mating between AA (chrysippus and dorippus) and aa (Danaus chrysippus alcippus), or heterozygote unfitness, or both.非洲的金斑蝶（Danaus chrysippus (L.)）包含四个基本隔离的半种群，这些半种群具有迁飞习性，并在非洲大陆东部和中部区域季节性地发生杂交。在杂交带（而非其他区域）中，该蝴蝶通常会被一种杀雄内共生细菌——螺原体属（Spiroplasma sp.）寄生，这种细菌主要感染肯尼亚境内的金斑蝶肯尼亚亚种（Danaus chrysippus chrysippus）。一种严格以母系方式遗传的W-常染色体易位突变，将B和C颜色基因座连接起来，使得这些基因座在chrysippus亚种中获得了性连锁特性。我们对肯尼亚内罗毕附近卡萨拉尼（Kasarani）地区从诱集植物上采集的野生卵繁育的成虫，开展了两段长期监测：第一段时长18个月（2004–2005年），第二段时长12个月（2009–2010年），监测内容为其性别比例以及A、C颜色基因座的基因型变异。此外，在2009–2010年期间，我们对所有存活的成虫进行了螺原体感染情况的筛查。卡萨拉尼的杂交种群在三个方面表现出高度的非典型性，且这种状态已持续约30年：其一，种群性别比例长期偏向雌性（符合预期），但存在季节性波动——当金斑蝶肯尼亚亚种（cc型）数量达到峰值时，雌雄比最低；当金斑蝶多里波斯亚种（Danaus chrysippus dorippus，CC型）占优时，雌雄比最高。其二，种群始终以雌雄两性的Cc杂合子为主，尤以雌性个体更为显著。其三，cc型雄性始终极为稀少，这是因为它们会被杀雄菌系统性杀灭；而CC基因型的个体则偏向雄性。正是这种性别与基因型的失衡，导致该种群严重偏离哈迪-温伯格平衡（Hardy–Weinberg equilibrium），部分原因在于cc型雌性几乎只能与C-型雄性交配。我们提出如下学术观点：其一，两性的Cc杂合子无法与任一亲本半种群一同扩散；其二，携带W-常染色体易位突变的螺原体阳性雌性，相较于未携带该易位的雌性具有选择优势；其三，内共生菌与该易位共同构成了一个“魔法性状”（magic trait）连锁群，这是金斑蝶肯尼亚亚种与多里波斯亚种之间形成全息基因组生殖隔离的基础；其四，多里波斯亚种中雄性占优的现象表明，该类个体必然拥有一种杀雄抑制基因来保护自身。与C基因座的情况不同，Aa杂合子始终处于显著且持久的缺失状态，这提示要么存在AA型（chrysippus和dorippus亚种）与aa型（金斑蝶阿尔西普斯亚种，Danaus chrysippus alcippus）之间的选型交配（assortative mating），要么存在杂合子适合度降低，或两者兼具。