Genomic data offers valuable insights into population history and species divergence, but interpreting complex evolutionary processes remains challenging, particularly in cases of recent divergence and ancestral polymorphism. This study addresses the taxonomic and evolutionary complexities of two endemic Hogna spider species from Madeira, H. maderiana from Porto Santo and H. insularum from Madeira, Desertas, Bugio, and Porto Santo, which exhibit mitochondrial gene tree discordance and ambiguous morphological boundaries. Using ddRADseq genomic data, population genomic analyses, and coalescent-based demographic analyses, we aim to determine whether these two nominal species represent a case of early divergence with unsorted molecular markers due to incomplete lineage sorting (ILS), if they are hybridising within the contact zone on the island of Porto Santo, or if they represent a single species exhibiting extreme morphological polymorphism. Our genetic structure analyses suggested three potential genetic clusters, one for each nominal species and one compatible with hybridisation between the two species on Porto Santo Island. However, demographic modelling and D-statistics rejected gene flow, instead supporting the existence of a third independent lineage in Porto Santo. The lack of genetic separation between these lineages likely reflects short recent divergence and unsorted ancestral polymorphisms. Our findings highlight the challenges of inferring hybridisation solely based on population structure analyses, which may lead to an overestimation of gene flow. This study highlights the importance of integrating demographic modelling and genetic data to resolve complex evolutionary histories and emphasizes the need for careful interpretation of genomic data to avoid misattributing gene flow.

Paula Escuer

and 4 more

The spider genus Dysdera has undergone a remarkable diversification in the oceanic archipelago of the Canary Islands, ~60 endemic species originated during the 20 million years since the origin of the archipelago. This evolutionary radiation has been accompanied by substantial dietary shifts, often characterized by phenotypic modifications encompassing morphological, metabolic and behavioral changes. Hence, these endemic spiders represent an excellent model for understanding the evolutionary drivers and to pinpoint the genomic determinants underlying adaptive radiations. Recently, we achieved the first chromosome-level genome assembly of one of the endemic species, D. silvatica, providing a high-quality reference sequence for evolutionary genomics studies. Here, we conducted a low-coverage based resequencing study of a natural population of D. silvatica from La Gomera island. Taking advantage of the new high-quality genome, we characterized genome-wide levels of nucleotide polymorphism, divergence, and linkage disequilibrium, and inferred the demographic history of this population. We also performed comprehensive genome-wide scans for recent positive selection. Our findings uncovered exceptionally high levels of nucleotide diversity and recombination in this geographically restricted endemic species, indicative of large historical effective population sizes. Furthermore, we identified genomic regions potentially under positive selection, shedding light on relevant biological processes, such as vision and nitrogen extraction as possible targets of adaptation and eventually, as drivers of the species diversification. This pioneering study in spiders endemic of an oceanic archipelago lays the groundwork for broader population genomics investigations aimed at understanding the genetic mechanisms driven adaptive radiations in island ecosystems.

Paula Escuer

and 7 more

We present the chromosome-level genome assembly of Dysdera silvatica Schmidt, 1981, a nocturnal ground-dwelling spider endemic from the Canary Islands. The genus Dysdera has undergone a remarkable diversification in this archipelago mostly associated with shifts in the level of trophic specialization, becoming an excellent model to study the genomic drivers of adaptive radiations. The new assembly (1.37 Gb; and scaffold N50 of 174.2 Mb), was performed using the chromosome conformation capture scaffolding technique, represents a continuity improvement of more than 4,500 times with respect to the previous version. The seven largest scaffolds or pseudochromosomes cover 87% of the total assembly size and match consistently with the seven chromosomes of the karyotype of this species, including the characteristic large X chromosome. To illustrate the value of this new resource we performed a comprehensive analysis of the two major arthropod chemoreceptor gene families (i.e., gustatory and ionotropic receptors). We identified 545 chemoreceptor sequences distributed across all pseudochromosomes, with a notable underrepresentation in the X chromosome. At least 54% of them localize in 83 genomic clusters with a significantly lower evolutionary distances between them than the average of the family, suggesting a recent origin of many of them. This chromosome-level assembly is the first high-quality genome representative of the Synspermiata clade, and just the third among spiders, representing a new valuable resource to gain insights into the structure and organization of chelicerate genomes, including the role that structural variants, repetitive elements and large gene families played in the extraordinary biology of spiders.