A genetic switch for male UV iridescence in an incipient species pair of sulphur butterflies

Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of ultraviolet (UV) iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern United States with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X (or large-Z) effect. Within this chromosome-wide reproductive barrier, linkage mapping indicates that cis-regulatory variation of bric a brac (bab) underlies the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knockout, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results highlight how a genetic switch can regulate a premating signal and integrate with other reproductive barriers during intermediate phases of speciation.

A genetic switch for male UV-iridescence in an incipient species pair of sulphur butterflies

Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of UV iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern US with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X effect. Within this chromosome-wide reproductive barrier, cis-regulatory variation of bric a brac (bab) drives the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knock-out, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results provide new insights into the diversification of sexual signals and the species concept.

Ability of Current Phylogenetic Clustering to Detect Speciation History

Phylogenetic diversity aims to quantify the evolutionary relatedness among the species comprising a community, using the phylogenetic tree as the metric of the evolutionary relationships. Could these measures unveil the evolutionary history of an area? For example, in a speciation hotspot (biodiversity cradle), we intuitively expect that the species in the community will be more phylogenetically clustered than randomly expected. Here, using a theoretical simulation model, we estimate the ability of phylogenetic metrics of current diversity to detect speciation history. We found that, in the absence of dispersal, if the incipient species do not coexist in the region of speciation (as expected under allopatric speciation), there was no clear phylogenetic clustering and phylogenetic diversity failed to detect speciation history. But if the incipient species coexisted (sympatric speciation), metrics such as standardized effect size of Faith’s Phylogenetic Diversity (PD) and of Mean Nearest Taxon Distance (MNTD) were able to identify areas of high speciation, while Mean Pairwise Distance (MPD) was a poor indicator. PD systematically outperformed MNTD. Dispersal was a game-changer. It allowed species to expand their range, colonize areas, and led to the coexistence of the incipient species originating from a common ancestor. If speciation gradient was spatially contiguous, dispersal strengthened the associations between phylogenetic clustering and speciation history. In the case of spatially random speciation, dispersal blurred the signal with phylogenetic clustering occurring in areas of low or no speciation. Our results imply that phylogenetic clustering is an indicator of speciation history only under certain conditions.

On the Trichoptera of Italy with delineation of incipient sibling species

Lumpers, focussing between gross and molecular morphologies and neglecting fine phenomics, highly underestimate biodiversity. The outdated lumper’s attitude fixed in the Distribution Atlas of European Trichoptera (Neu et al. 2018) is revisited and some theoretical background of why and how to delineate phylogenetic-retigenetic incipient species is outlined very briefly. We expose the adverse effect of lumpers in order to improve by fine phenomics the detection of the fine structure of the local genetic resources, the most valuable and most specific living components, the endemics of the particular ecosystems. In the Italian caddisfly fauna we have recorded, treated or revised the species complex status of Plectrocnemia geniculata, Tinodes dives, Diplectrona atra, Rhyacophila praemorsa, R. pubescens, R. vulgaris, Drusus graecus, D. discolor D. muelleri, D. flavipennis, D. mixtus, D. spelaeus, D. alpinus, D. nebulicola, Limnephilus stigma. Raised the subspecies status to phylogenetic-retigenetic incipient species rank of Plectrocnemia calabrica Malicky, 1971 stat. nov., Tinodes cantabricus Botosaneanau & Gonzalez, 2001 stat. restit., stat. nov., Tinodes consiglioi Botosaneanu, 1980 stat. nov. Tinodes jeekeli Botosaneanu, 1980, stat restit., stat. nov., Ernodes romaniulus Moretti, Cianficconi, Campadelli & Crudele, 1999 stat. nov. Described 21 new species: Wormaldia ameliae sp. nov., W. dupla sp. nov., W. joani sp. nov., W. marilouae sp. nov., W. reggella sp. nov., W. toscanica sp. nov., Diplectrona ligurica sp. nov., Rhyacophila abruzzica sp. nov., R. harmasa sp. nov., R. ligurica sp. nov., R. pilosa sp. nov., Drusus oblos sp. nov., D. cerreto sp. nov., D. dondenaz sp. nov., D. tagolt sp. nov., D. hatras sp. nov., D. granparadiso sp. nov., D. camposilvano sp. nov., Limnephilus logos sp. nov., Chaetopteryx kimera sp. nov., Consorophylax juliae sp. nov.

The limits to parapatric speciation 3: evolution of strong reproductive isolation in presence of gene flow despite limited ecological differentiation

Gene flow tends to impede the accumulation of genetic divergence. Here, we determine the limits for the evolution of postzygotic reproductive isolation in a model of two populations that are connected by gene flow. We consider two selective mechanisms for the creation and maintenance of a genetic barrier: local adaptation leads to divergence among incipient species due to selection against migrants, and Dobzhansky–Muller incompatibilities (DMIs) reinforce the genetic barrier through selection against hybrids. In particular, we are interested in the maximum strength of the barrier under a limited amount of local adaptation, a challenge that many incipient species may initially face. We first confirm that with classical two-locus DMIs, the maximum amount of local adaptation is indeed a limit to the strength of a genetic barrier. However, with three or more loci and cryptic epistasis, this limit holds no longer. In particular, we identify a minimal configuration of three epistatically interacting mutations that is sufficient to confer strong reproductive isolation. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

DNA-based species delimitation reveals cryptic and incipient species in synchronous flashing fireflies (Coleoptera: Lampyridae) of Southeast Asia

Synchronous flashing fireflies of the genus Pteroptyx are ubiquitous throughout Southeast Asia, yet fundamental knowledge about their biodiversity is lacking. Recent studies have revealed notable population-level phylogeographical structure within the Pteroptyx tener and P. bearni groups in Malaysia, suggesting that cryptic species may exist. Additionally, morphological and genetic similarities between P. balingiana and P. malaccae have raised questions about the former’s validity as a distinct species. We collected samples from previously unsampled populations and assembled the most comprehensive genetic dataset for Pteroptyx to date, to characterize species boundaries within the P. tener, P. bearni and P. malaccae groups. Using a suite of species delimitation analyses, we show that P. tener along the west coast of Peninsular Malaysia (PM) is distinct from populations from the east coast and Borneo despite the absence of morphological differentiation. However, analyses could not conclusively differentiate P. bearni from Borneo and eastern PM, nor identify P. balingiana and P. malaccae as distinct species, indicating that these populations may be conspecific or represent incipient species. This study underlines the need to increase geographical, taxonomic and genetic sampling of Southeast Asian fireflies to provide a better understanding of their biodiversity.

Selection and gene flow define polygenic barriers between incipient butterfly species

Characterizing the genetic architecture of species boundaries remains a difficult task. Hybridizing species provide a powerful system to identify the factors that shape genomic variation and, ultimately, identify the regions of the genome that maintain species boundaries. Unfortunately, complex histories of isolation, admixture and selection can generate heterogenous genomic landscapes of divergence which make inferences about the regions that are responsible for species boundaries problematic. However, as the signal of admixture and selection on genomic loci varies with recombination rate, their relationship can be used to infer their relative importance during speciation. Here, we explore patterns of genomic divergence, admixture and recombination rate among hybridizing lineages across the Heliconius erato radiation. We focus on the incipient species, H. erato and H. himera, and distinguish the processes that drive genomic divergence across three contact zones where they frequently hybridize. Using demographic modeling and simulations, we infer that periods of isolation and selection have been major causes of genome-wide correlation patterns between recombination rate and divergence between these incipient species. Upon secondary contact, we found surprisingly highly asymmetrical introgression between the species pair, with a paucity of H. erato alleles introgressing into the H. himera genomes. We suggest that this signal may result from a current polygenic species boundary between the hybridizing lineages. These results contribute to a growing appreciation for the importance of polygenic architectures of species boundaries and pervasive genome-wide selection during the early stages of speciation with gene flow.

The limits to parapatric speciation 3: Evolution of strong reproductive isolation in presence of gene flow despite limited ecological differentiation

Gene flow tends to impede the accumulation of genetic divergence. Here, we determine the limits for the evolution of postzygotic reproductive isolation in a model of two populations that are connected by gene flow. We consider two selective mechanisms for the creation and maintenance of a genetic barrier: local adaptation leads to divergence among incipient species due to selection against migrants, and Dobzhansky-Muller incompatibilities (DMIs) reinforce the genetic barrier through selection against hybrids. In particular, we are interested in the maximum strength of the barrier under a limited amount of local adaptation, a challenge that may initially face many incipient species. We first confirm that with classical two-locus DMIs, the maximum amount of local adaptation is indeed a limit to the strength of a genetic barrier. However, with three or more loci and cryptic epistasis, this limit holds no longer. In particular, we identify a minimal configuration of three epistatically interacting mutations that is sufficient to confer strong reproductive isolation.