Heliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Müllerian mimicry and mating behavior. Their rapid radiation has been strongly influenced by hybridization, which has created new species and allowed sharing of color patterning alleles between mimetic species pairs. While these processes have frequently been observed in widespread species with contiguous distributions, many Heliconius species inhabit patchy or rare habitats that may strongly influence the origin and spread of species and color patterns. Here, we assess the effects of historical population fragmentation and unique biology on the origins, genetic health, and color pattern evolution of two rare and sparsely distributed Brazilian butterflies, Heliconius hermathena and Heliconius nattereri. We assembled genomes and re-sequenced whole genomes of eight H. nattereri and 71 H. hermathena individuals. These species harbor little genetic diversity, skewed site frequency spectra, and high deleterious mutation loads consistent with recent population bottlenecks. Heliconius hermathena consists of discrete, strongly isolated populations that likely arose from a single population that dispersed after the last glacial maximum. Despite having a unique color pattern combination that suggested a hybrid origin, we found no genome-wide evidence that H. hermathena is a hybrid species. However, H. hermathena mimicry evolved via introgression, from co-mimetic Heliconius erato, of a small genomic region upstream of the color patterning gene cortex. Heliconius hermathena and H. nattereri population fragmentation, potentially driven by historical climate change and recent deforestation, has significantly reduced the genetic health of these rare species. Our results contribute to a growing body of evidence that introgression of color patterning alleles between co-mimetic species appears to be a general feature of Heliconius evolution.

中文翻译：

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杂交和栖息地破碎化在巴西神秘的长翅蝴蝶Heliconius nattereri和H.hermathena进化中的作用。

Heliconius蝴蝶广泛分布于新热带地区，并演化出令人惊叹的机翼颜色图案，可调节穆勒人的模仿和交配行为。它们的快速辐射受到杂交的强烈影响，杂交产生了新物种，并允许在模拟物种对之间共享彩色图案等位基因。尽管经常在具有连续分布的广泛物种中观察到这些过程，但许多Heliconius物种居住在斑驳或稀有的栖息地中，这些栖息地可能强烈影响物种和颜色模式的起源和传播。在这里，我们评估了历史种群分裂和独特生物学对两种稀有且稀疏分布的巴西蝴蝶Heliconius hermathena和Heliconius nattereri的起源，遗传健康和颜色模式演变的影响。我们组装了8个n.Hatternattereri和71个h.hermathena个体的基因组并重新测序了整个基因组。这些物种几乎没有遗传多样性，偏斜的位点频谱以及与近期种群瓶颈相一致的高有害突变负荷。Heliconius hermathena由离散的，高度孤立的种群组成，这些种群很可能是由最后一个冰期最大值之后分散的单个种群引起的。尽管有独特的颜色模式组合暗示了杂种起源，但我们没有发现全基因组证据表明H. hermathena是杂种。然而，H.hermathena的拟态是通过从共拟Heliconius erato渗入到彩色图案基因皮质上游的一个小基因组区域而进化而来的。Heliconius hermathena和H.nattereri种群分裂，由于可能受到历史气候变化和近期森林砍伐的驱动，大大降低了这些稀有物种的遗传健康。我们的研究结果为越来越多的证据表明，仿拟物种之间的彩色图案等位基因渗入似乎是Heliconius进化的一般特征。