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Downloaded the Edelman Alignment; Smaller P Values Suggest That There Is Stronger Alignment from Dryad ( Massardo et al. BMC Biology (2020) 18:84 https://doi.org/10.1186/s12915-020-00797-1 RESEARCH ARTICLE Open Access The roles of hybridization and habitat fragmentation in the evolution of Brazil’s enigmatic longwing butterflies, Heliconius nattereri and H. hermathena Darli Massardo1†, Nicholas W. VanKuren1*† , Sumitha Nallu1, Renato R. Ramos2, Pedro G. Ribeiro3, Karina L. Silva-Brandão4, Marcelo M. Brandão3, Marília B. Lion5, André V. L. Freitas2, Márcio Z. Cardoso5 and Marcus R. Kronforst1* Abstract Background: 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. Results: 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. Conclusions: 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. Keywords: Heliconius, Hybridization, Introgression, Mutation load, Mimicry, Phylogenetics * Correspondence: [email protected]; [email protected] †Darli Massardo and Nicholas W. VanKuren contributed equally to this work. 1Department of Ecology & Evolution, The University of Chicago, Chicago, IL, USA Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Massardo et al. BMC Biology (2020) 18:84 Page 2 of 21 Background described the systematics, biogeography, natural history, Butterflies have served as a historically significant model ecology, and behavior of this species. More recently, of insect diversity because of the group’s extreme species Seixas et al. [26] described the population ecology of H. diversity, containing an estimated 18,000 species, and hermathena based on a 14-month mark-recapture ex- the even more striking color pattern diversity that de- periment. Heliconius hermathena is associated with fines the subspecies, races, forms, and morphs of many white sand habitats (campina and campinarana) butterfly species. Among butterflies, the Neotropical throughout the Brazilian Amazon. These patchy, harsh genus Heliconius has attracted attention for centuries environments produce a network of seven described H. because of their bold and highly variable wing color pat- hermathena subspecies, including H. hermathena curua, terns [1–4], as well as their fascinating behavior and nat- which was just described in 2019 [27]. Six H. her- ural history, which includes co-evolved relationships mathena subspecies display subtle variations on a with larval host plants, widespread Müllerian mimicry, shared, putatively non-mimetic color pattern (Fig. 1) adult pollen feeding, and pupal-mating behavior [2, 4– while the seventh subspecies, vereatta, lacks much of the 6]. Today, researchers are leveraging the natural diversity yellow patterning on the fore- and hindwings and is a of Heliconius butterflies and genomic tools to co-mimic of sympatric Heliconius erato and Heliconius characterize the molecular genetic basis of mimicry [7– melpomene. Heliconius hermathena vereatta has a lim- 13] and track genome-wide patterns of differentiation ited spatial distribution and is known to freely hybridize and introgression associated with speciation [14–20]. with adjacent Heliconius hermathena duckei near the Yet, for all of the attention, a number of fascinating Heli- town of Faro in the State of Pará [25]. Based on the conius species have evaded modern genomic interroga- phenotypic variation among individuals and color pat- tion. Two particularly striking examples are Heliconius tern frequencies in the field, Brown and Benson [25] in- nattereri and Heliconius hermathena from Brazil. ferred that mimicry in H. hermathena was controlled by Heliconius nattereri is an exceptionally rare, geograph- a single locus with a dominant, melanic allele. The gen- ically restricted species found only along a section of etics of mimicry in H. hermathena has not been further Brazil’s Atlantic Forest spanning portions of the states of explored. The evolutionary origin of H. hermathena it- Espírito Santo and Bahia [21–23]. Heliconius nattereri self is a topic of interest. The non-mimetic color pattern stands out relative to other species in the genus because shared by most H. hermathena subspecies appears to be it is the only Heliconius species that is endangered [24] a combination of features from close relatives H. erato and it is also the only Heliconius species with pro- and H. charithonia, and Hewitson [28] reflected this no- nounced sexually dimorphic color patterns (Fig. 1). Fe- ticeable mixture when naming the species. Today, there male H. nattereri display a black, yellow, and orange are a number of well-characterized instances of intro- “tiger stripe” pattern that facilitates mimicry with other gression and hybrid speciation in Heliconius [15, 19, 20, co-occurring Heliconius and Ithomiini species while 29], and while H. hermathena is considered one possible males display a non-mimetic yellow and black wing pat- example of hybrid speciation [30–32], the evolutionary tern. Prior to Keith Brown’s rediscovery of H. nattereri origin of this species remains largely unexplored. in the 1960s [21, 22], this species was only known from As part of an international collaboration, we have been approximately 20 pinned specimens in museums around studying the biology, genomics, and population genetics the world. Furthermore, males and females had not been of Brazil’s endemic, and enigmatic, Heliconius fauna. collected together, and because of their pronounced sex- With permission and funding from the Brazilian govern- ual dimorphism in both color pattern and behavior, fe- ment, we have performed new surveys of H. nattereri males had been historically described as a different [23] and H. hermathena [27] populations, collected sam- species, H. fruhstorferi Riffarth, 1899. In the 1960s and ples, and performed genomic analyses. Here, we present 1970s, Brown and colleagues extensively surveyed the reference genome sequences and whole-genome rese- range of H. nattereri, discovering additional localities quencing datasets for both species. We use these data to and specimens, including one large population that they infer their modern population structure and historical studied intensively for three years. Based on his work, demography relative to other well-studied and wide- Brown was not optimistic about the long-term future of spread Heliconius species, characterize the genomic con- H. nattereri because of its limited and still dwindling sequences of population decline and historical habitat habitat and his observations that it seemed to be an “in- fragmentation, and define the genetic basis of mimicry flexible” and “sensitive” species [22]. in H. hermathena and trace its evolutionary origin. Like H. nattereri, H. hermathena has historically been These data add to a growing list of genomic resources
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