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.2019 Aug 1;11(8):2136-2150.
doi: 10.1093/gbe/evz113.

Genome-wide SNP Data Reveal an Overestimation of Species Diversity in a Group of Hawkmoths

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Genome-wide SNP Data Reveal an Overestimation of Species Diversity in a Group of Hawkmoths

Anna K Hundsdoerfer et al. Genome Biol Evol..

Abstract

The interface between populations and evolving young species continues to generate much contemporary debate in systematics depending on the species concept(s) applied but which ultimately reduces to the fundamental question of "when do nondiscrete entities become distinct, mutually exclusive evolutionary units"? Species are perceived as critical biological entities, and the discovery and naming of new species is perceived by many authors as a major research aim for assessing current biodiversity before much of it becomes extinct. However, less attention is given to determining whether these names represent valid biological entities because this is perceived as both a laborious chore and an undesirable research outcome. The charismatic spurge hawkmoths (Hyles euphorbiae complex, HEC) offer an opportunity to study this less fashionable aspect of systematics. To elucidate this intriguing systematic challenge, we analyzed over 10,000 ddRAD single nucleotide polymorphisms from 62 individuals using coalescent-based and population genomic methodology. These genome-wide data reveal a clear overestimation of (sub)species-level diversity and demonstrate that the HEC taxonomy has been seriously oversplit. We conclude that only one valid species name should be retained for the entire HEC, namely Hyles euphorbiae, and we do not recognize any formal subspecies or other taxonomic subdivisions within it. Although the adoption of genetic tools has frequently revealed morphologically cryptic diversity, the converse, taxonomic oversplitting of species, is generally (and wrongly in our opinion) accepted as rare. Furthermore, taxonomic oversplitting is most likely to have taken place in intensively studied popular and charismatic organisms such as the HEC.

Keywords: RAD-sequencing; gene flow; oversplitting; speciation; species delineation; taxonomy.

© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

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Figures

<sc>Fig</sc>. 1.
Fig. 1.
—Geographical distribution of the HEC. Geographical sampling of HEC populations mapped onto an annual mean temperature map using ArcGIS Desktop v.10.3. Temperature data were derived from WorldClim and mapped at 1-km2 spatial resolution with a temporal range of ∼1950–2010. Colors of circles ascribe sample sites to the five species of the currently valid taxonomy. Dashed white lines separate the two morphological species groups based onHyles euphorbiae (north) andHyles tithymali (south) and enclose the areas with larvae of intermediate morphology (includingHyles cretica andHyles sammuti).
<sc>Fig</sc>. 2.
Fig. 2.
—Phylogenetic hypothesis and HEC population structuring. Phylogenetic relationships and population structuring of the HEC including two specimens ofHyles dahlii (HEC s.l.) as outgroup based on thec85m6 data matrix, which consisted of 10,093 unlinked SNPs in 2,174,137 bp. (a) ML tree inferred from RAxML analysis. The maximal internal distance of 2% within the HEC is found between ecITA_7697 (Italy) and SLK_5684 (Slovakia). Branch support was inferred with 500 bootstrap replicates; bootstrap values are indicated above each branch. (b) Admixture graphs ofK = 2–5 source populations. The blue color was chosen to refer toHyles euphorbiae, the other four colors (brown, orange, dark green, and pink) distinguish four further possible groups but have not been coded to refer to taxonomy or phylogeny. (c) Individual cluster assignment probabilities for theK = 2 ordered by geographical distribution. Population abbreviations correspond to figure 1. Abbreviations refer to species definitions according to currently valid taxonomy: c,Hyles cretica; e,H. euphorbiae; r,Hyles robertsi; s,Hyles sammuti; and t,Hyles tithymali. The colors coding this taxonomy correspond to those in figure 1.
<sc>Fig</sc>. 3.
Fig. 3.
—SVDquartets coalescence analyses. The broad gray branches show the SVDquartets species tree according to valid taxonomy based on thec85m30 sequence data matrix, which consisted of 835 unlinked SNPs in 160,778 bp (outgroupHyles dahlii pruned). We overlaid the lineage tree and positioned the individuals according to species affiliation by extending their branches by hand to illustrate gene flow. Bootstrap support values above 80% are shown at nodes (there are only two: one value 89 in the species tree in large font size supporting the crown group ofHyles cretica,Hyles robertsi, andHyles euphorbiae, and one value 87 in the lineages tree in smaller font size). The taxonomy color code corresponds to that in figure 1.
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