Hybrid speciation driven by multilocus introgression of ecological traits.

Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species1,2. However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation3. Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus, which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene, and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus. These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture.

The butterflies (Lepidoptera, Papilionoidea) of the Parque Estadual Intervales and surroundings, São Paulo, Brazil / As borboletas (Lepidoptera, Papilionoidea) do Parque Estadual Intervales e arredores, São Paulo, Brasil

Abstract The Global South has witnessed increasing sampling of its immense biological diversity during the past century. However, the diversity of many regions remains unknown, even at pristine and highly threatened places, such as in the Atlantic Forest; and for bioindicator, umbrella, and flagship groups. The present study reports the first butterfly list of the Parque Estadual Intervales, São Paulo, Brazil and surroundings, a key protected area in the last massive continuous of the Atlantic Forest. We compiled data from museums and four years of field work, under three sampling methods. We also aimed at providing resources to support conservation efforts by analyzing 27 years of climatic data (detailed in the Supplementary Material, in English and in Portuguese), discussing our results also for non-academics, and producing scientific outreach and educational material. A companion article dealt with the experiences of science outreach and capacity development, and illustrated the butterfly catalogue of the species sampled in the park. We found 312 species that sum to 2,139 records. The museum had 229 species (432 records), and we sampled 142 species (1,682 individuals), in a total effort of 36,679 sampling hours (36,432 trap and 247 net and observation hours). The richest families were Nymphalidae (148 species) and Hesperiidae (100 species). Most species were sampled exclusively by active methods (79.8%), but other sources (passive sampling, citizen science, etc.) also found unique records. We found the highest diversity metrics from January to May, and we demonstrated that winter months had less richness and abundance. We illustrated the 20 species common to all regions, and listed those that were found more than seven months in the year, as well as the most abundant species in trap sampling, with forest dwellers as well as species common to open and fragmented areas. The dominant species in our trap datasets was the iridescent white morpho, Morpho epistrophus (Fabricius, 1796), and we suggest it to become the park butterfly mascot.

Resumo O Sul Global testemunhou crescente amostragem de sua imensa diversidade biológica durante o século passado. Entretanto, a diversidade de muitas regiões permanece desconhecida, mesmo em locais pristinos e altamente ameaçados, como na Mata Atlântica; e para grupos bioindicadores, guarda-chuva e emblemáticos. O presente estudo reporta a primeira lista de borboletas do Parque Estadual Intervales, São Paulo, Brasil e arredores, uma unidade de conservação chave no último maciço contínuo de Mata Atlântica. Compilamos dados de museus e quatro anos de campo, sob três métodos de amostragem. Também visamos oferecer recursos para apoiar os esforços de conservação, analisando 27 anos de dados climáticos (detalhados no Material Suplementar, em inglês e em português), discutindo nossos resultados numa linguagem também para não acadêmicos, e produzindo material de divulgação científica e educativos. Um artigo irmão tratou das experiências de divulgação científica e capacitação, e ilustrou o catálogo de borboletas das espécies amostradas no parque. Encontramos 312 espécies em 2.139 registros. O museu tinha 229 espécies (432 registros), e amostramos 142 espécies (1.682 indivíduos), em um esforço total de 36.679 horas de amostragem (36.432 armadilhas e 247 horas de rede e observação). As famílias mais ricas foram Nymphalidae (148 espécies) e Hesperiidae (100 espécies). A maioria das espécies foi amostrada exclusivamente por métodos ativos (79,8%), mas outras fontes (passiva, ciência cidadã, etc.) também encontraram registros únicos. Encontramos as maiores métricas de diversidade de janeiro a maio, e demonstramos que os meses de inverno tiveram menos riqueza e abundância. Ilustramos as 20 espécies comuns a todas as regiões, e listamos aquelas que foram encontradas em mais de sete meses no ano, bem como as espécies mais abundantes em armadilhas, com espécies florestais e também comuns em áreas abertas e fragmentadas. A espécie dominante em nossas armadilhas foi a morfo branca iridescente, Morpho epistrophus (Fabricius, 1796), e sugerimos que se torne a borboleta mascote do parque.

Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait.

BACKGROUND: The origin and modification of novel traits are important aspects of biological diversification. Studies combining concepts and approaches of developmental genetics and evolutionary biology have uncovered many examples of the recruitment, or co-option, of genes conserved across lineages for the formation of novel, lineage-restricted traits. However, little is known about the evolutionary history of the recruitment of those genes, and of the relationship between them -for example, whether the co-option involves whole or parts of existing networks, or whether it occurs by redeployment of individual genes with de novo rewiring. We use a model novel trait, color pattern elements on butterfly wings called eyespots, to explore these questions. Eyespots have greatly diversified under natural and sexual selection, and their formation involves genetic circuitries shared across insects. RESULTS: We investigated the evolutionary history of the recruitment and co-recruitment of four conserved transcription regulators to the larval wing disc region where circular pattern elements develop. The co-localization of Antennapedia, Notch, Distal-less, and Spalt with presumptive (eye)spot organizers was examined in 13 butterfly species, providing the largest comparative dataset available for the system. We found variation between families, between subfamilies, and between tribes. Phylogenetic reconstructions by parsimony and maximum likelihood methods revealed an unambiguous evolutionary history only for Antennapedia, with a resolved single origin of eyespot-associated expression, and many homoplastic events for Notch, Distal-less, and Spalt. The flexibility in the (co-)recruitment of the targeted genes includes cases where different gene combinations are associated with morphologically similar eyespots, as well as cases where identical protein combinations are associated with very different phenotypes. CONCLUSIONS: The evolutionary history of gene (co-)recruitment is consistent with both divergence from a recruited putative ancestral network, and with independent co-option of individual genes. The diversity in the combinations of genes expressed in association with eyespot formation does not parallel diversity in characteristics of the adult phenotype. We discuss these results in the context of inferring homology. Our study underscores the importance of widening the representation of phylogenetic, morphological, and genetic diversity in order to establish general principles about the mechanisms behind the evolution of novel traits.

Skull modularity in neotropical marsupials and monkeys: size variation and evolutionary constraint and flexibility.

An organism is built through a series of contingent factors, yet it is determined by historical, physical, and developmental constraints. A constraint should not be understood as an absolute obstacle to evolution, as it may also generate new possibilities for evolutionary change. Modularity is, in this context, an important way of organizing biological information and has been recognized as a central concept in evolutionary biology bridging on developmental, genetics, morphological, biochemical, and physiological studies. In this article, we explore how modularity affects the evolution of a complex system in two mammalian lineages by analyzing correlation, variance/covariance, and residual matrices (without size variation). We use the multivariate response to selection equation to simulate the behavior of Eutheria and Metharia skulls in terms of their evolutionary flexibility and constraints. We relate these results to classical approaches based on morphological integration tests based on functional/developmental hypotheses. Eutherians (Neotropical primates) showed smaller magnitudes of integration compared with Metatheria (didelphids) and also skull modules more clearly delimited. Didelphids showed higher magnitudes of integration and their modularity is strongly influenced by within-groups size variation to a degree that evolutionary responses are basically aligned with size variation. Primates still have a good portion of the total variation based on size; however, their enhanced modularization allows a broader spectrum of responses, more similar to the selection gradients applied (enhanced flexibility). Without size variation, both groups become much more similar in terms of modularity patterns and magnitudes and, consequently, in their evolutionary flexibility.