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Seixas, F. A.

Publications and source records attributed to Seixas, F. A..

7 recordsLinked to original sources

Temperature-dependent and sex-specific phenotypic plasticity in Heliconius charithonia

External environmental cues can influence the development trajectory of organisms and lead to the formation of distinct phenotypes from the same genotype. Phenotypic plasticity is common in Lepidoptera, with temperature frequently playing a key role. The zebra-longwing (Heliconius charithonia) gets its name from its characteristic black wings with yellow stripes. In some populations, yellow scales are sometimes partially replaced by orange ( rusty) scales. The proportion of individuals with rusty scales varies geographically and individuals within the same population can vary drastically for this phenotype. Whether such variation is genetically encoded, or environment-dependent is not known. Here we test the influence of temperature in producing the rusty scales phenotype, as well as on the developmental rates, weight, and mortality in this species. Only female butterflies reared in warm controlled conditions develop rusty scales on the yellow parts of their wings. However, under more extreme (warmer) conditions, both males and females exhibit pronounced rusty scale phenotypes, indicating a sexually dimorphic response to temperature that affects both sexes. This temperature-sensitive trait can be triggered during both larval and pupal stages. Temperature also affects life-history traits, and we observed a trade-off between developmental rate and mortality. Individuals raised in warmer conditions develop more rapidly than those in cooler environments, but this accelerated growth is accompanied by higher mortality across all developmental stages.

developmental biology↗

Ancient inversion polymorphisms are locally adaptive in a widespread butterfly species

Wide-ranging species are subject to varying biotic and abiotic selection pressures across their distribution. While local adaptation does not manifest in obvious morphological changes, population genomic studies can reveal cryptic diversity and provide insights into local adaptive processes. In this study, we investigated the biogeographic history and genomic diversity across the range of the zebra longwing butterfly Heliconius charithonia, a species with a widespread distribution in the Neotropics, but which is phenotypically homogenous across its range. We examined whole genome sequence data from 55 individuals from the eight described subspecies. We infer that there were at least two distinct colonization events of the Caribbean islands from the mainland. The second colonization wave occurred relatively recently, accounting for the genetic homogeneity observed across the species range. Despite low divergence across most of the genome, two large non-recombining genomic regions showed deeply divergent haplotypes that correspond to chromosomal inversions. Phylogenetic analyses indicate ancient origins of these inversion polymorphisms, and there is no evidence that they were introgressed from another extant lineage of Heliconius. These ancient polymorphisms are likely maintained by heterogeneous selection across the landscape, with the inversion on chromosome 19 likely playing a role in local adaptation to cold and desiccation. Our findings underscore the importance of genomic analysis in uncovering hidden diversity and adaptation in phenotypically homogenous species and highlight the significant role of chromosomal inversions in driving local adaptation.

evolutionary biology↗

Genomics of Neotropical biodiversity indicators: two butterfly radiations with rampant chromosomal rearrangements and hybridisation

A major question in evolutionary biology is what drives the diversification of lineages. Rapid, recent radiations are ideal systems for addressing how new species arise because they still show key morphological and ecological adaptations associated with speciation. While most studied recent radiations have evolved in an insular environment, less research has been carried out on continental radiations with complex species interactions. Melinaea and Mechanitis butterflies (Nymphalidae: Ithomiini) have rapidly radiated in the Neotropics. They are classical models for Amazonian biogeography and colour pattern mimicry and have been proposed as biodiversity indicators. We generated reference genomes for five species of each genus, and whole-genome resequencing data of most species and subspecies covering a wide geographic range to assess phylogeographic relationships, patterns of hybridisation and chromosomal rearrangements. Our data help resolve the classification of these taxonomically challenging butterflies and reveal very high diversification rates. We find rampant evidence of historical hybridisation and putative hybrid species in both radiations, which may have facilitated their rapid diversification. Moreover, dozens of chromosomal fusions and fissions were identified between congeneric species, and even some within species. We conclude that interactions between geography, hybridisation and chromosomal rearrangements have contributed to these two rapid radiations in the highly diverse Neotropical region. We suggest that rapid radiations may be spurred by repeated periods of geographic isolation during Pleistocene climate oscillations, combined with lineage-specific rapid accumulation of incompatibilities during allopatric phases, followed by secondary contact with some gene exchange. Significance StatementUnderstanding factors contributing to rapid speciation is a key aim of evolutionary biology. Here we focus on two rapid radiations of Neotropical butterflies. Our genomic data with broad taxonomic and geographic coverage reveal rampant hybridisation and chromosomal rearrangements, each likely contributing to the high diversification rates. Our study highlights the use of genomic data to resolve taxonomically challenging species groups and elucidate drivers of diversification in rapid radiations. We show that for biodiversity hotspots with recent radiations, barcoding is insufficient to characterise species richness due to gene flow and recent speciation. The taxonomic implications of both introgression and karyotype diversity for species delimitation are important to consider during monitoring and management of biodiversity in these vulnerable habitats.

evolutionary biology↗

Major patterns in the introgression history of Heliconius butterflies

AO_SCPLOWBSTRACTC_SCPLOWGene flow between species is an important evolutionary process that can facilitate adaptation and lead to species diversification. It also makes reconstruction of species relationships difficult. Here, we use the full-likelihood multispecies coalescent (MSC) approach to estimate species phylogeny and major introgression events in Heliconius butterflies from whole-genome sequence data. We obtain a robust estimate of species branching order among major clades in the genus, including the "melpomene-silvaniform" group, which shows extensive historical and on-going gene flow. We obtain chromosome-level estimates of key parameters in the species phylogeny, including species divergence times, present-day and ancestral population sizes as well as the direction, timing, and intensity of gene flow. Our analysis leads to a phylogeny with introgression events that differ from those obtained in previous studies. We find that H. aoede most likely represents the earliest-branching lineage of the genus and that "silvaniform" species are paraphyletic within the melpomene-silvaniform group. Our phylogeny provides new, parsimonious histories for the origins of key traits in Heliconius, including pollen feeding and an inversion involved in wing pattern mimicry. Our results demonstrate the power and feasibility of the full-likelihood MSC approach for estimating species phylogeny and key population parameters despite extensive gene flow. The methods used here should be useful for analysis of other difficult species groups with high rates of introgression.

evolutionary biology↗

Complex basis of hybrid female sterility and Haldane's rule in Heliconius butterflies: Z-linkage and epistasis

Hybrids between diverging populations are often sterile or inviable. Hybrid unfitness usually evolves first in the heterogametic sex - a pattern known as Haldanes rule. The genetics of Haldanes Rule have been extensively studied in species where the male is the heterogametic (XX/XY) sex, but its basis in taxa where the female is heterogametic (ZW/ZZ), such as Lepidoptera and birds, is largely unknown. Here, we analyse a new case of female hybrid sterility between geographic subspecies of Heliconius pardalinus. The two subspecies mate freely in captivity, but female F1 hybrids in both directions of cross are sterile. Sterility is due to arrested development of oocytes after they become differentiated from nurse cells, but before yolk deposition. We backcrossed fertile male F1 hybrids to parental females, and mapped quantitative trait loci (QTLs) for female sterility. We also identified genes differentially expressed in the ovary, and as a function of oocyte development. The Z chromosome has a major effect, similar to the "large X effect" in Drosophila, with strong epistatic interactions between loci at either end of the Z chromosome, and between the Z chromosome and autosomal loci on chromosomes 8 and 20. Among loci differentially expressed between females with arrested vs. non-arrested ovary development, we identified six candidate genes known also from Drosophila melanogaster and Parage aegeria oogenesis. This study is the first to characterize hybrid sterility using genome mapping in the Lepidoptera. We demonstrate that sterility is produced by multiple complex epistastic interactions often involving the sex chromosome, as predicted by the dominance theory of Haldanes Rule.

evolutionary biology↗

Complex introgression history of the erato-sara clade of Heliconius butterflies

AO_SCPLOWBSTRACTC_SCPLOWIntrogressive hybridization plays a key role in adaptive evolution and species diversification in many groups of species. However, frequent hybridization and gene flow between species makes estimation of the species phylogeny and key population parameters challenging. Here, we show that by accounting for phasing and using full-likelihood analysis methods, introgression histories and population parameters can be estimated reliably from whole-genome sequence data. We employ full-likelihood methods under the multispecies coalescent (MSC) model with and without gene flow to analyze the genomic data from six members of the erato-sara clade of Heliconius butterflies and infer the species phylogeny and cross-species introgression events. The methods naturally accommodate random fluctuations in genealogical history across the genome due to deep coalescence. To avoid heterozygote phasing errors in haploid sequences commonly produced by genome assembly methods, we process and compile unphased diploid sequence alignments and use analytical methods to average over uncertainties in heterozygote phase resolution. There is robust evidence for introgression across the genome, both among distantly related species deep in the phylogeny and between sister species in shallow parts of the tree. We obtain chromosome-specific estimates of key population parameters such as introgression directions, times and probabilities, as well as species divergence times and population sizes for modern and ancestral species. We confirm ancestral gene flow between the sara clade and an ancestral population of H. telesiphe, a likely hybrid speciation origin for H. hecalesia, and gene flow between sister species H. erato and H. himera. Inferred introgression among ancestral species also explains the history of two chromosomal inversions deep in the phylogeny of the group. This study illustrates how a full-likelihood approach based on the multispecies coalescent makes it possible to extract rich historical information of species divergence and gene flow from genomic data.

evolutionary biology↗

Synteny-based genome assembly for 16 species of Heliconius butterflies, and an assessment of structural variation across the genus

Heliconius butterflies (Lepidoptera: Nymphalidae) are a group of 48 neotropical species widely studied in evolutionary research. Despite the wealth of genomic data generated in past years, chromosomal level genome assemblies currently exist for only two species, Heliconius melpomene and H. erato, each a representative of one of the two major clades of the genus. Here, we use these reference genomes to improve the contiguity of previously published draft genome assemblies of 16 Heliconius species. Using a reference-assisted scaffolding approach, we place and order the scaffolds of these genomes onto chromosomes, resulting in 95.7-99.9% of their genomes anchored to chromosomes. Genome sizes are somewhat variable among species (270-422 Mb) and in one small group of species (H. hecale, H. elevatus and H. pardalinus) differences in genome size are mainly driven by a few restricted repetitive regions. Genes within these repeat regions show an increase in exon copy number, an absence of internal stop codons, evidence of constraint on non-synonymous changes, and increased expression, all of which suggest that the extra copies are functional. Finally, we conducted a systematic search for inversions and identified five moderately large inversions fixed between the two major Heliconius clades. We infer that one of these inversions was transferred by introgression between the lineages leading to the erato/sara and burneyi/doris clades. These reference-guided assemblies represent a major improvement in Heliconius genomic resources that should aid further genetic and evolutionary studies in this genus.

genomics↗