The roles of hybridization and habitat fragmentation in the evolution of Brazil's enigmatic longwing butterflies, Heliconius nattereri and H. hermathena

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Massardo, Darli ^[1] ; VanKuren, Nicholas W. ^[1] ; Nallu, Sumitha ^[1] ; Ramos, Renato R. ^{[2, 3]} ; Ribeiro, Pedro G. ^[4] ; Silva-Brandao, Karina L. ^[5] ; Brandao, Marcelo M. ^[4] ; Lion, Marilia B. ^[6] ; Freitas, Andre V. L. ^{[2, 3]} ; Cardoso, Marcio Z. ^[6] ; Kronforst, Marcus R. ^[1]

Afiliação do(s) autor(es)

^[1] Univ Chicago, Dept Ecol & Evolut, Chicago, IL 60637 - USA

^[2] Univ Estadual Campinas, Inst Biol, Dept Biol Anim, Campinas, SP - Brazil

^[3] Univ Estadual Campinas, Inst Biol, Museu Zool, Campinas, SP - Brazil

^[4] Univ Estadual Campinas, Ctr Biol Mol & Engn Genet, Campinas, SP - Brazil

^[5] Univ Fed ABC, Ctr Ciencias Nat & Humanas, Santo Andre, SP - Brazil

^[6] Univ Fed Rio Grande do Norte, Dept Ecol, Natal, RN - Brazil

• Tipo de documento: Artigo Científico
• Fonte: BMC Biology; v. 18, n. 1 JUL 3 2020.
• Citações Web of Science: 0

Resumo

BackgroundHeliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Mullerian 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.ResultsWe 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.ConclusionsHeliconius 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. (AU)

• Processo FAPESP: 12/50260-6 - Estruturação e evolução da biota amazônica e seu ambiente: uma abordagem integrativa
• Beneficiário: Lúcia Garcez Lohmann
• Modalidade de apoio: Auxílio à Pesquisa - Programa BIOTA - Temático
• Processo FAPESP: 12/16266-7 - Genômica populacional: uma nova abordagem para estudos de especiação em insetos devido ao uso de hospedeiros aplicada ao desenvolvimento de estratégias sustentáveis de MIP
• Beneficiário: Karina Lucas da Silva-Brandão
• Modalidade de apoio: Auxílio à Pesquisa - Jovens Pesquisadores
• Processo FAPESP: 11/00417-3 - Biologia de sistemas aplicada a agricultura: análise de transcriptomas e interactomas
• Beneficiário: Marcelo Mendes Brandao
• Modalidade de apoio: Auxílio à Pesquisa - Jovens Pesquisadores
• Processo FAPESP: 11/50225-3 - História natural, filogenia e conservação de lepidópteros neotropicais
• Beneficiário: André Victor Lucci Freitas
• Modalidade de apoio: Auxílio à Pesquisa - Programa BIOTA - Regular