SONATA 18 [2022/47/D/NZ8/01956]

• Scientific goal of the project

Although it is commonly acknowledged that species represent a unique level of self-organising entities in nature, their delineation as well as understanding the mechanism underlying speciation is often difficult, and this process becomes even more problematic if speciation is incomplete. The transition from one species to another is one of the main issues in evolutionary biology. It is commonly accepted that speciation occurs across a continuum over time, however, the various points along the process need to be studied in order to understand the nature of this phenomenon and dividing speciation into stages could help to better understand the entire process. Presently, it is generally acknowledged that allopatric speciation (a model in which separation is caused by emerging barriers) is the main driving force behind speciation, while parapatric (no specific extrinsic barrier to gene flow) and, in particular, sympatric speciation (no barrier but also no large-scale geographic distance to reduce gene flow between individuals of the same population) models still cause a lot of controversy and are not recognized by a significant part of the scientific community.

Biogeography is a key component in understanding speciation as it affects geographic isolation and gene flow, under which reproductive isolation creates new biodiversity. Reduced gene flow plays a critical role in speciation, which has traditionally been divided into three major modes depending upon the spatial distribution of diverging populations. However, although it seems quite a common scenario that a single mode was solely involved in the separation of two taxa, there is new evidence for the hypothesis of mixed modes of speciation, in which the geographic context and levels of gene flow temporally vary during the divergence process. Ring species are a special case of parapatric speciation, where the original population spreads in two directions around a significant geographic barrier (encircling it); although neighbouring populations around the ring show free exchange of genes, at a single location two adjacent populations are reproductively isolated, though there is still a potential gene flow between each population.

Arid regions are characterised by relatively fewer species compared to the better-watered biomes, but also by high levels of endemism, and particularly high functional diversity. While this makes them unique regions regarding biodiversity conservation, they are still poorly understood. This especially concerns the Central Asian Arid Zone (CAAZ: approx. 50–110°N and 35–50°E). In these ancient landscapes (the steppe-desert of Central Asia has existed since the Eocene), which are particularly climate sensitive, patterns of radiation and evolution for biomes and animals have occurred at different periods of time, with cold arid periods during glacial maxima spurring diversification, and these vulnerable areas now are important hotspots for the conservation of certain plant and animal species.

Numerous studies have shown that flightless, sedentary arthropods (especially apterous insects) can serve as excellent models for evolutionary studies, and that their phylogenesis may more often reflect their history of colonisation. Central Asian representatives of the tribe Dorcadionini Swainson, 1840 (Coleoptera: Cerambycidae), a taxonomically highly complex group that includes numerous described species and subspecies, are endemic to the region, making them a perfect model group for inferring the geographic modes of speciation and revealing the evolutionary and ecological mechanisms that underlie the generation of biodiversity of the CAAZ. While it would not cause much controversy in a region with clear geographical barriers, such as mountain ranges or large rivers, most of the distribution area of these beetles is localised within the flat terrain without such barriers. Yet, this group is highly diverse and includes taxa that are usually very difficult to distinguish.

This project aims at building the first large-scale, time calibrated phylogeny of Central Asian Dorcadionini, and by applying a total evidence approach, at reconstructing the most likely evolutionary scenarios that have been driving the speciation of this characteristic group. The results will also serve as a general model for other apterous arthropod groups distributed or evolved in this vast region and will lay the foundations for the genesis of the CAAZ fauna.

• Ring species

A term of ring species, or circle of races, is commonly understood as a connected series of neighbouring populations distributed around a physical barrier, such as a large lake, where each of them interbreeds with closely sited related populations. An original population spreads in two directions around the barrier (encircling it); although neighbouring populations around the ring show free exchange of genes, at a single location two adjacent populations are reproductively isolated, though there is still potential gene flow between each population (Irwin et al. 2001; Coyne & Orr 2004) (Fig. 6). As the consequence, those “terminal” populations, non-breeding but genetically connected, may co-exist in the same region in sympatry, thus closing the “ring”. Although the concept of ring species was initially considered as a special case of allopatric speciation, Coyne and Orr (2004) argue that Mayr's original conception describes, in fact, “speciation occurring through the attenuation of gene flow with distance”, and that ring species provide evidence of parapatric speciation in a non-conventional sense. According to these authors, ring species are more convincing than cases of clinal isolation in showing that gene flow hampers the evolution of reproductive isolation. While in the case of clinal isolation, reproductive isolation was caused by environmental differences that increase with the distance between populations, similar argumentation cannot be used for ring species as the most reproductively isolated populations occur in the same habitat. This model is based on the fact that interfertility is not a transitive relation, which means that if population A breeds with population B, and B breeds with population C, it does not mean that populations A and C can interbreed. Even though that ring species are a counterexample to the transitivity of interbreeding, it is unclear whether any of the studied cases actually permit gene flow from one edge of a population to the other. Despite a few seemingly perfect cases of this phenomenon—in North American salamanders and a bird, greenish warbler, species complex around the Tibetan Plateau—all ultimately failed to fully meet the definition. Hence, properly documented examples of ring species are still lacking. Given the very peculiar distribution of a few Dorcadionini species (groups) around large Central Asian lakes, particularly eight “subspecies” of Dorcadion semenovi around the Issyk-Kul Lake in NE Kyrgyzstan (but also other taxa around the Kazakh Lake Balkhash and Mongolian Uvs Lake), it seems likely that one of these cases will finally fully support the theory of ring species. Populations of these beetles are usually distributed around a lake in "enclaves" of Stipa clumps (their host plants), however, there are typically no physical barriers between them and a small part of populations is believed to travel longer distances in search of new niches, therefore although gene exchange is still possible, advantageous conditions for limiting gene flow are maintained.

• Cerambycidae and its highly speciose tribe Dorcadionini

Longhorned beetles or cerambycids, with approx. 35,000 described species (Tavakilian & Chevillotte 2021), is one of the most abundant families in the largest and most diverse order of animals—beetles (Coleoptera). Despite the great diversity of these beetles and their economic and biocenotic importance as wood pests, plant pollinators, and deadwood decompositors, these organisms are far from being well understood. Although due to the variety of forms and colours, they attract the attention of numerous entomologists, there are very few scientists globally who truly study this group and the evolutionary mechanisms that drive its speciation. This especially applies to the region of Central Asia and the tribe Dorcadionini, which is a highly speciose cerambycid group (approx. 900 species and subspecies) and one of the most challenging in terms of species identification owing to a large number of taxa, intraspecific variability or similarity between species. This Palaearctic tribe is divided into five (Tavakilian & Chevillotte 2021) or six (Danilevsky 2020) genera, and it associates highly diverse, flightless species. Central Asian Dorcadionini involve two endemic to this region genera: Eodorcadion Breuning, 1947 (approx. 70 taxa) and Politodorcadion Danilevsky, 1996 (12 taxa), as well as the representatives of two subgenera of the nominative and widely distributed genus Dorcadion Dalman, 1817: Acutodorcadion Danilevsky, Kasatkin & Rubenyan, 2005 (approx. 60 taxa) and Dorcadion Dalman, 1817 (approx. 40 taxa). Since these beetles are flightless—which is quite unique in the family—they have evolved many local forms that are extremely difficult to distinguish due to the subtle differences in their morphology, e.g., in elytral and pronotal colour pattern, which consists of a few wide stripes on each elytron made of white (or whitish) pubescence. Various designs of this sunflower shell-like pattern are very common in all genera across the tribe and likely arose independently in different species groups, in different regions, by parallel speciation (in most species groups, some taxa are uniformly black or brown in both sexes, which suggests this is not a homologous trait).

These fascinating beetles are also one of the best examples where species-richness hampers the phylogenetic reconstruction, making this group extremely challenging for systematic and evolutionary studies (Dascălu et al. 2021). Regarding the taxonomy, only one genus of the tribe, Eodorcadion, has already been revised (Danilevsky 2007) but even this study was based solely on morphological characters and lacks any phylogenetic analysis. Earlier, Danilevsky et al. (2005) used endophallic morphology to introduce some taxonomic changes in the tribe.