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A comprehensive phylogeography of the Hyles euphorbiae complex (Lepidoptera: Sphingidae) indicates a 'glacial refuge belt'.

ABSTRACT: We test the morphology based hypothesis that the Western Palaearctic spurge hawkmoths represent two species, the Eurasian H. euphorbiae and Afro-Macaronesian H. tithymali. It has been suggested that these species merged into several hybrid swarm populations, although a mitochondrial phylogeography revealed substructure with local differentiation. We analysed a three-gene mt-dataset (889 individuals) and 12 microsatellite loci (892 individuals). Microsatellite analyses revealed an overall weak differentiation and corroborated the superordinate division into two clusters. The data indicate that the populations studied belong to only one species according to the biological species concept, refuting the opening hypothesis. A future taxonomic revision appears necessary to reflect the division into two subgroups. Ancestral mitochondrial polymorphisms are retained in H. euphorbiae, indicating gene flow within a broad 'glacial refuge belt' and ongoing postglacial gene flow. Diverse patterns of extensive mito-nuclear discordance in the Mediterranean and the Middle East presumably evolved by more recent processes. This discordance indicates introgression of H. tithymali-related mitochondrial haplogroups, accompanied (to a lesser degree) by nuclear alleles, into Italian and Aegean H. euphorbiae populations as recently as the late Holocene. The complex mosaic of divergence and reintegration is assumed to have been influenced by locally differing environmental barriers to gene flow.

SUBMITTER: Mende MB

PROVIDER: S-EPMC4954964 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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A comprehensive phylogeography of the Hyles euphorbiae complex (Lepidoptera: Sphingidae) indicates a 'glacial refuge belt'.

Mende Michael B MB Bartel Manuela M Hundsdoerfer Anna K AK

Scientific reports 20160721

We test the morphology based hypothesis that the Western Palaearctic spurge hawkmoths represent two species, the Eurasian H. euphorbiae and Afro-Macaronesian H. tithymali. It has been suggested that these species merged into several hybrid swarm populations, although a mitochondrial phylogeography revealed substructure with local differentiation. We analysed a three-gene mt-dataset (889 individuals) and 12 microsatellite loci (892 individuals). Microsatellite analyses revealed an overall weak di ...[more]

PMID: 27439775

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Project description:BackgroundMitochondrial genes are among the most commonly used markers in studies of species' phylogeography and to draw conclusions about taxonomy. The Hyles euphorbiae complex (HEC) comprises six distinct mitochondrial lineages in the Mediterranean region, of which one exhibits a cryptic disjunct distribution. The predominant mitochondrial lineage in most of Europe, euphorbiae, is also present on Malta; however, it is nowadays strangely absent from Southern Italy and Sicily, where it is replaced by 'italica'. A separate biological entity in Italy is further corroborated by larval colour patterns with a congruent, confined suture zone along the Northern Apennines. By means of historic DNA extracted from museum specimens, we aimed to investigate the evolution of the mitochondrial demographic structure of the HEC in Italy and Malta throughout the Twentieth Century.ResultsAt the beginning of the Twentieth Century, the European mainland lineages were also present at a moderate frequency in Southern Italy and Sicily. The proportion of 'italica' then steadily increased in this area from below 60 percent to near fixation in about 120 years. Thus, geographical sorting of mitochondrial lineages in the HEC was not as complete then as the current demography suggests. The pattern of an integral 'italica' core region and a disjunct euphorbiae distribution evolved very recently. To explain these strong demographic changes, we propose genetic drift due to anthropogenic habitat loss and fragmentation in combination with an impact from recent climate warming that favoured the spreading of the potentially better adapted 'italica' populations.ConclusionsThe pattern of geographically separated mitochondrial lineages is commonly interpreted as representing long term separated entities. However, our results indicate that such a pattern can emerge surprisingly quickly, even in a widespread and rather common taxon. We thus caution against drawing hasty taxonomic conclusions from biogeographical patterns of mitochondrial markers derived from modern sampling alone.

Project description:BackgroundMorphological and traditional genetic studies of the young Pliocene genus Hyles have led to the understanding that despite its importance for taxonomy, phenotypic similarity of wing patterns does not correlate with phylogenetic relationship. To gain insights into various aspects of speciation in the Spurge Hawkmoth (Hyles euphorbiae), we assembled a chromosome-level genome and investigated some of its characteristics.ResultsThe genome of a male H. euphorbiae was sequenced using PacBio and Hi-C data, yielding a 504 Mb assembly (scaffold N50 of 18.2 Mb) with 99.9% of data represented by the 29 largest scaffolds forming the haploid chromosome set. Consistent with this, FISH analysis of the karyotype revealed n = 29 chromosomes and a WZ/ZZ (female/male) sex chromosome system. Estimates of chromosome length based on the karyotype image provided an additional quality metric of assembled chromosome size. Rescaffolding the published male H. vespertilio genome resulted in a high-quality assembly (651 Mb, scaffold N50 of 22 Mb) with 98% of sequence data in the 29 chromosomes. The larger genome size of H. vespertilio (average 1C DNA value of 562 Mb) was accompanied by a proportional increase in repeats from 45% in H. euphorbiae (measured as 472 Mb) to almost 55% in H. vespertilio. Several wing pattern genes were found on the same chromosomes in the two species, with varying amounts and positions of repetitive elements and inversions possibly corrupting their function.ConclusionsOur two-fold comparative genomics approach revealed high gene synteny of the Hyles genomes to other Sphingidae and high correspondence to intact Merian elements, the ancestral linkage groups of Lepidoptera, with the exception of three simple fusion events. We propose a standardized approach for genome taxonomy using nucleotide homology via scaffold chaining as the primary tool combined with Oxford plots based on Merian elements to infer and visualize directionality of chromosomal rearrangements. The identification of wing pattern genes promises future understanding of the evolution of forewing patterns in the genus Hyles, although further sequencing data from more individuals are needed. The genomic data obtained provide additional reliable references for further comparative studies in hawkmoths (Sphingidae).

Dataset Information

A comprehensive phylogeography of the Hyles euphorbiae complex (Lepidoptera: Sphingidae) indicates a 'glacial refuge belt'.

Publications

A comprehensive phylogeography of the Hyles euphorbiae complex (Lepidoptera: Sphingidae) indicates a 'glacial refuge belt'.

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