Genomic data reveal deep genetic structure but no support for current taxonomic designation in a grasshopper species complex

Taxonomy has traditionally relied on morphological and ecological traits to interpret and classify biological diversity. Over the last decade, technological advances and conceptual developments in the field of molecular ecology and systematics have eased the generation of genomic data and changed the paradigm of biodiversity analysis. Here we illustrate how traditional taxonomy has led to species designations that are supported neither by high throughput sequencing data nor by the quantitative integration of genomic information with other sources of evidence. Specifically, we focus on Omocestus antigai and Omocestus navasi, two montane grasshoppers from the Pyrenean region that were originally described based on quantitative phenotypic differences and distinct habitat associations (alpine vs. Mediterranean-montane habitats). To validate current taxonomic designations, test species boundaries, and understand the factors that have contributed to genetic divergence, we obtained phenotypic (geometric morphometrics) and genome-wide SNP data (ddRADSeq) from populations covering the entire known distribution of the two taxa. Coalescent-based phylogenetic reconstructions, integrative Bayesian model-based species delimitation, and landscape genetic analyses revealed that populations assigned to the two taxa show a spatial distribution of genetic variation that do not match with current taxonomic designations and is incompatible with ecological/environmental speciation. Our results support little phenotypic variation among populations and a marked genetic structure that is mostly explained by geographic distances and limited population connectivity across the abrupt landscapes characterizing the study region. Overall, this study highlights the importance of integrative approaches to identify taxonomic units and elucidate the evolutionary history of species

Hierarchical genetic structure shaped by topography in a narrow-endemic montane grasshopper

[Background]: Understanding the underlying processes shaping spatial patterns of genetic structure in free-ranging organisms is a central topic in evolutionary biology. Here, we aim to disentangle the relative importance of neutral (i.e. genetic drift) and local adaptation (i.e. ecological divergence) processes in the evolution of spatial genetic structure of the Morales grasshopper (Chorthippus saulcyi moralesi), a narrow-endemic taxon restricted to the Central Pyrenees. More specifically, we analysed range-wide patterns of genetic structure and tested whether they were shaped by geography (isolation-by-distance, IBD), topographic complexity and present and past habitat suitability models (isolation-byresistance, IBR), and environmental dissimilarity (isolation-by-environment, IBE).[Results]: Different clustering analyses revealed a deep genetic structure that was best explained by IBR based on topographic complexity. Our analyses did not reveal a significant role of IBE, a fact that may be due to low environmental variation among populations and/or consequence of other ecological factors not considered in this study are involved in local adaptation processes. IBR scenarios informed by current and past climate distribution models did not show either a significant impact on genetic differentiation after controlling for the effects of topographic complexity, which may indicate that they are not capturing well microhabitat structure in the present or the genetic signal left by dispersal routes defined by habitat corridors in the past.[Conclusions]: Overall, these results indicate that spatial patterns of genetic variation in our study system are primarily explained by neutral divergence and migration-drift equilibrium due to limited dispersal across abrupt reliefs, whereas environmental variation or spatial heterogeneity in habitat suitability associated with the complex topography of the region had no significant effect on genetic discontinuities after controlling for geography. Our study highlights the importance of considering a comprehensive suite of potential isolating mechanisms and analytical approaches in order to get robust inferences on the processes promoting genetic divergence of natural populations.VN was supported by a FPI pre-doctoral scholarship (BES-2012-053741) from Ministerio de Economía y Competitividad. JO was supported by Severo Ochoa (SEV-2012-0262) and Ramón y Cajal (RYC-2013-12501) research fellowships. This work received financial support from research grants CGL2011-25053 (Ministerio de Ciencia e Innovación and European Social Fund), POII10-0197-0167, PEII-2014-023-P (Junta de Comunidades de Castilla-La Mancha and European Social Fund) and UNCM08-1E-018 (European Regional Development Fund).We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).Peer reviewe