Two robust rules have been discovered about animal hybrids: Heterogametic hybrids are more unfit (Haldane’s rule), and sex chromosomes are disproportionately involved in hybrid incompatibility (the large-X/Z effect). The exact mechanisms causing these rules in female heterogametic taxa such as butterflies are unknown but are suggested by theory to involve dominance on the sex chromosome. We investigate hybrid incompatibilities adhering to both rules in
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Papilio andHeliconius butterflies and show that dominance theory cannot explain our data. Instead, many defects coincide with unbalanced multilocus introgression between the Z chromosome and all autosomes. Our polygenic explanation predicts both rules because the imbalance is likely greater in heterogametic females, and the proportion of introgressed ancestry is more variable on the Z chromosome. We also show that mapping traits polygenic on a single chromosome in backcrosses can generate spurious large-effect QTLs. This mirage is caused by statistical linkage among polygenes that inflates estimated effect sizes. By controlling for statistical linkage, most incompatibility QTLs in our hybrid crosses are consistent with a polygenic basis. Since the two genera are very distantly related, polygenic hybrid incompatibilities are likely common in butterflies.Free, publicly-accessible full text available October 31, 2024 -
Abstract Reproductive isolation is the heuristic basis of the biological species concept, but what is it? Westram et al. (this issue) propose that it is a measurable quantity, “barrier strength,” that prevents gene flow among populations. However, their attempt to make the concept of reproductive isolation more scientific is unlikely to satisfy the diverse opinions of all evolutionary biologists. There are many different opinions about the nature of species, even under the biological species concept. Complete reproductive isolation, where gene flow is effectively zero, is regarded by some biologists as an important end point of speciation. Others, including Westram et al., argue for a more nuanced approach, and they also suggest that reproductive isolation may differ in different parts of the genome due to variation in genetic linkage to divergently selected loci. In contrast to both these approaches, we favour as a key criterion of speciation the stable coexistence of divergent populations in sympatry. Obviously, such populations must be reproductively isolated in some sense, but neither the fraction of the genome that is exchanged, nor measures of overall barrier strength acting on neutral variation will yield very precise predictions as to species status. Although an overall measure of reproductive isolation is virtually unattainable for these reasons, its early generation components, such as assortative mating, divergent selection, or hybrid inviability and sterility are readily measurable and remain informative. For example, we can make the prediction that to remain divergent in sympatry, almost all sexual species will require strong assortative mating, as well as some sort of ecological or intrinsic selection against hybrids and introgressed variants.more » « less
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Abstract Transposable elements (TEs) play major roles in the evolution of genome structure and function. However, because of their repetitive nature, they are difficult to annotate and discovering the specific roles they may play in a lineage can be a daunting task. Heliconiine butterflies are models for the study of multiple evolutionary processes including phenotype evolution and hybridization. We attempted to determine how TEs may play a role in the diversification of genomes within this clade by performing a detailed examination of TE content and accumulation in 19 species whose genomes were recently sequenced. We found that TE content has diverged substantially and rapidly in the time since several subclades shared a common ancestor with each lineage harboring a unique TE repertoire. Several novel SINE lineages have been established that are restricted to a subset of species. Furthermore, the previously described SINE, Metulj, appears to have gone extinct in two subclades while expanding to significant numbers in others. This diversity in TE content and activity has the potential to impact how heliconiine butterflies continue to evolve and diverge.more » « less
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Abstract Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies, ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life.more » « less
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Abstract Aim The biodiversity crisis has highlighted the need to assess and map biodiversity in order to prioritize conservation efforts. Clearwing butterflies (tribe Ithomiini) have been proposed as biological indicators for habitat quality in Neotropical forests, which contain the world's richest biological communities. Here, we provide maps of different facets of Ithomiini diversity across the Neotropics to identify areas of evolutionary and ecological importance for conservation and evaluate their overlap with current anthropogenic threats.
Location Neotropics.
Methods We ran species distribution models on a data set based on 28,986 georeferenced occurrences representing 388 ithomiine species to generate maps of geographic rarity, taxonomic, phylogenetic and Müllerian mimetic wing pattern diversity. We quantified and mapped the overlap of diversity hotspots with areas threatened by or providing refuge from current anthropogenic pressures.
Results The eastern slopes of the Andes formed the primary hotspot of taxonomic, phylogenetic and mimetic diversity, with secondary hotspots in Central America and the Atlantic Forest. Most diversity indices were strongly spatially correlated. Nevertheless, species‐poor communities on the Pacific slopes of the Andes also sheltered some of the geographically rarest species. Overall, tropical montane forests that host high species and mimetic diversity as well as rare species and mimicry rings appeared particularly under threat.
Main conclusions Remote parts of the Upper Amazon may act as refuges against current anthropogenic pressures for a limited portion of Ithomiini diversity. Furthermore, it is likely that the current threat status may worsen with ongoing climate change and deforestation. In this context, the tropical Andes occupy a crucial position as the primary hotspot for multiple facets of biodiversity for ithomiine butterflies, as they do for angiosperms, tetrapods and other insect taxa. Our results support the role of ithomiine butterflies as a suitable flagship indicator group for Neotropical butterfly diversity and reinforce the position of the tropical Andes as a flagship region for biodiversity conservation in general, and insect and butterfly conservation in particular.
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We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating
Heliconius butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgressed loci are underrepresented in low-recombination and gene-rich regions, consistent with the purging of foreign alleles more tightly linked to incompatibility loci. Here, we identify a hitherto unknown inversion that traps a color pattern switch locus. We infer that this inversion was transferred between lineages by introgression and is convergent with a similar rearrangement in another part of the genus. These multiple de novo genome sequences enable improved understanding of the importance of introgression and selective processes in adaptive radiation. -
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Abstract Aim The landscape of the Neotropical region has undergone dynamic evolution throughout the Miocene, with the extensive Pebas wetland occupying western Amazonia between 23 and
c . 10 Ma and the continuous uplift of the Andes mountains. The complex interaction between the Andes and Amazonia probably influenced the trajectory of Neotropical biodiversity, but evidence from time‐calibrated phylogenies of groups that diversified during this period is lacking. We investigate the role of these landscape transformations in the dynamics of diversification in the Neotropical region using a 26‐Myr‐old endemic butterfly radiation.Location Neotropics.
Time period Oligocene to present.
Major taxa studied Ithomiini butterflies.
Methods We generated one of the most comprehensive time‐calibrated molecular phylogenies of a large clade of Neotropical insects, the butterfly tribe Ithomiini, comprising 340 species (87% of extant species) and spanning 26 Myr of diversification. We applied a large array of birth–death models and historical biogeography estimations to assess the dynamics of diversification and biotic interchanges, especially at the Amazonia–Andes interface.
Results Our results suggest that the Amazonian Pebas wetland system played a major role in the timing and geography of diversification of Ithomiini, by constraining dispersal and diversification in the Amazon basin until
c . 10 Ma. During the Pebas wetland period, Ithomiini diversification mostly took place in the Andes, where terrestrial habitats were not affected. An explosion of interchanges with Amazonia and with the Northern Andes accompanied the demise of the Pebas system (11–8 Ma) and was followed by local diversification in those areas, which led to a substantial renewal of diversification.Main conclusions Many studies on Neotropical diversity have focused only on the Andes, whereas we show that it is the waxing and waning of the Pebas mega‐wetland, interacting with Andean uplift, that determined the timing and patterns of regional interchanges and diversification in Ithomiini.
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Abstract Understanding why species richness peaks along the Andes is a fundamental question in the study of Neotropical biodiversity. Several biogeographic and diversification scenarios have been proposed in the literature, but there is confusion about the processes underlying each scenario, and assessing their relative contribution is not straightforward. Here, we propose to refine these scenarios into a framework which evaluates four evolutionary mechanisms: higher speciation rate in the Andes, lower extinction rates in the Andes, older colonization times and higher colonization rates of the Andes from adjacent areas. We apply this framework to a species‐rich subtribe of Neotropical butterflies whose diversity peaks in the Andes, the Godyridina (Nymphalidae: Ithomiini). We generated a time‐calibrated phylogeny of the Godyridina and fitted time‐dependent diversification models. Using trait‐dependent diversification models and ancestral state reconstruction methods we then compared different biogeographic scenarios. We found strong evidence that the rates of colonization into the Andes were higher than the other way round. Those colonizations and the subsequent local diversification at equal rates in the Andes and in non‐Andean regions mechanically increased the species richness of Andean regions compared to that of non‐Andean regions (‘species‐attractor’ hypothesis). We also found support for increasing speciation rates associated with Andean lineages. Our work highlights the importance of the Andean slopes in repeatedly attracting non‐Andean lineages, most likely as a result of the diversity of habitats and/or host plants. Applying this analytical framework to other clades will bring important insights into the evolutionary mechanisms underlying the most species‐rich biodiversity hotspot on the planet.
