bioRxiv Science⌕ Search

Biology subjects

Rosser, N.

Publications and source records attributed to Rosser, N..

6 recordsLinked to original sources

Genetic parallelism underpins convergent mimicry coloration across Lepidoptera

Convergent evolution, the repeated evolution of similar phenotypes in response to the same selective pressures across multiple lineages, is widespread in nature. The extent to which the same genetic mechanisms contribute to convergent evolution could reveal whether the pathway towards these optimal endpoints is flexible or constrained to follow a particular route. Although mimicry of aposematic colour patterns is well known in Lepidoptera, our knowledge of the genetic basis of these convergent patterns is mostly restricted to a few closely-related species. Here we study the genetic basis of mimicry across seven species of Ithomiini and Heliconius butterflies and a day-flying Chetone moth, representing lineages that diverged between [~]1-120 Mya, each presenting similar colour pattern switches. In all the butterfly species, the genetic variants most strongly associated with convergent colour pattern switches are similarly located in non-coding regions near the genes ivory and optix. Colour pattern variation in the moth is associated with a [~]1 Mb inversion around ivory paralleling the supergene architecture of the co-mimic Heliconius numata. In contrast to previous studies in Heliconius, there is limited evidence of alleles shared by means of hybridization in convergence among closely-related ithomiine species. Repeated parallel evolution of regulatory switches via reuse of the same two genes suggests that convergent colour pattern evolution is highly constrained, even across large evolutionary timescales.

evolutionary biology↗

Müllerian mimicry in Neotropical butterflies: One mimicry ring to bring them all, and in the jungle bind them

Understanding the mechanisms underlying species distributions and coexistence is essential to predict and prevent the impacts of global change, particularly in biodiversity hotspots. However, the effects of biotic interactions may be challenging to investigate at large spatial scales. Leveraging well-characterized Mullerian mimetic systems in Neotropical butterflies, we investigated spatial patterns of mutualistic mimetic interactions within and between two tribes of aposematic Nymphalid butterflies: the Heliconiini (Heliconiinae) and the Ithomiini (Danainae). Despite 85 My of independent evolutionary histories, many species share similar warning wing patterns across the Neotropics. In this study we show that both tribes form similar biodiversity hotspots with a high prevalence of rare species and mimetic patterns in the tropical Andes. However, we reveal a higher relative richness of heliconiine butterflies than ithomiines in the Amazon basin contrasting with the Andean concentration of ithomiine diversity. Despite this difference in broadscale diversity patterns, we also document large-scale spatial associations among phenotypically similar species within and between tribes, thereby providing new empirical evidence for Fritz Mullers historical model of mutualistic mimicry at a continental scale. Furthermore, comparative phylogenetic analyses suggest that co-mimetic species within and between tribes have converged towards similar climatic niches as a response to selection favoring co-occurrence. Our findings illustrate the strength of mutualistic interactions in shaping biodiversity patterns at continental scale and in supporting niche convergence even across millions of years of evolution. Critically, it also emphasizes the pervasive vulnerability of mimetic communities, bound by positive interactions, to disassembly induced by climate change. Significance statementMullerian mimicry is a remarkable example of convergent evolution driven by natural selection where coexisting prey species converge in their warning signal advertising their defenses to predators. Heliconiine and ithomiine butterflies found throughout Neotropical rainforests were instrumental in Fritz Mullers historical model, which provided the mechanism for such resemblance. Leveraging decades of fieldwork and museum collections, we show that species with similar color patterns present strikingly similar spatial distributions, regardless of how closely related they are. Such co-occurrence appears reinforced by the evolution of similar climatic requirements among look-alike species. Our findings emphasize the key role of mutualistic interactions in shaping large-scale patterns of biodiversity and supporting convergence in the climatic niches of species spanning across phylogenetically distant clades.

evolutionary 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↗

Cycad phylogeny predicts host plant use of Eumaeus butterflies

Eumaeus butterflies are obligate herbivores of Zamia, the most diverse neotropical genus of cycads. Eumaeus-Zamia interactions have been mainly characterized for species distributed in North and Central America. However, host plant use by the southern Eumaeus clade remains largely unknown, precluding a comprehensive study of co-evolution between the genera. Here, we combine fieldwork with museum and literature surveys to expand herbivory records for Eumaeus from 21 to 38 Zamia species. We inferred a time-calibrated phylogeny of Eumaeus to test for distinct macroevolutionary scenarios of host plant conservatism and co-evolution. We found remarkable coincidence between Eumaeus and Zamia diversification, with the butterfly stem group diverging at the same time as the most recent radiation of Zamia in the Miocene. Cophylogenetic reconciliation analyses show a strong cophylogenetic signal between cycads and their butterfly herbivores. Bipartite model-based approaches indicate that this is because closely related Zamia species are used by the same Eumaeus species, suggesting host plant resource tracking by the butterfly herbivores. Our results highlight a case of tight evolution between Eumaeus butterflies and cycads, pointing to the generality of correlated evolution and phylogenetic tracking in plant-herbivore interactions across seed plants.

evolutionary biology↗

Diverse genetic architectures on the Z chromosome underlie the two rules of speciation in Papilio butterfly hybrids

The fitness of animal hybrids follows two empirical rules: hybrids of the heterogametic sex aremore unfit (Haldanes Rule), and the sex chromosome is disproportionately involved in incompatibility (the large-X/Z effect). Whether these rules result from genetic mechanisms shared across taxa remains unknown, and existing explanations rarely consider female heterogametic taxa such as butterflies. Here, we investigate hybrid incompatibilities in Papilio and Heliconius butterflies, and show that defects coincide with unbalanced introgression between the Z chromosome and its genetic background. This polygenic mechanism predicts both rules because introgressed ancestry on the Z chromosome is more skewed in females, and is more variable than on all autosomes. Therefore, the explanation for both rules in butterflies shares little similarity with prevailing theories relying on dominance.

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↗