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Integrative taxonomy refutes a species hypothesis: The asymmetric hybrid origin of Arsapnia arapahoe (Plecoptera, Capniidae).

ABSTRACT: Molecular tools are commonly directed at refining taxonomies and the species that constitute their fundamental units. This has been especially insightful for groups for which species hypotheses are ambiguous and have largely been based on morphological differences between certain life stages or sexes, and has added importance when taxa are a focus of conservation efforts. Here, we examine the taxonomic status of Arsapnia arapahoe, a winter stonefly in the family Capniidae that is a species of conservation concern because of its limited abundance and restricted range in northern Colorado, USA. Phylogenetic analyses of sequences of mitochondrial and nuclear genes of this and other capniid stoneflies from this region and elsewhere in western North America indicated extensive haplotype sharing, limited genetic differences, and a lack of reciprocal monophyly between A. arapahoe and the sympatric A. decepta, despite distinctive and consistent morphological differences in the sexual apparatus of males of both species. Analyses of autosomal and sex-linked single nucleotide polymorphisms detected using genotyping by sequencing indicated that all individuals of A. arapahoe consisted of F₁ hybrids between female A. decepta and males of another sympatric stonefly, Capnia gracilaria. Rather than constitute a self-sustaining evolutionary lineage, A. arapahoe appears to represent the product of nonintrogressive hybridization in the limited area of syntopy between two widely distributed taxa. This offers a cautionary tale for taxonomists and conservation biologists working on the less-studied components of the global fauna.

SUBMITTER: Young MK

PROVIDER: S-EPMC6374720 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The study of complementary sources of biological variation (e.g. morphological, molecular) has allowed a better understanding of biodiversity through the construction of an integrative taxonomy. Using this approach, specimens from the Paranapiacaba Mountains, southeastern Brazil, were studied to update the knowledge on the stonefly family Perlidae from the region, characterize the species, and make associations between nymphs and adults using a fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene. The study also discusses the implications of integrative taxonomy and teneral specimens for the study of South American Perlidae. The molecular data were analyzed using Bayesian inference, Neighbor-joining, and delimiting species methods. Our results revealed that, in general, there was a morphological and molecular congruence between species. In the Paranapiacaba Mountains, three genera and 15 species were recorded: Anacroneuria boraceiensis Froehlich 2004, A. debilis (Pictet 1841) (new record), A. fiorentini De Ribeiro and Froehlich 2007 (new record), A. flintorum Froehlich 2002, A. iporanga Bispo and Froehlich 2004, A. itajaimirim Bispo and Froehlich 2004, A. polita (Burmeister 1913), A. subcostalis Klapálek 1921, A. tupi Bispo and Froehlich 2004 (with a description of the nymph), Kempnyia auberti Froehlich 1996, K. colossica (Navás 1934), K. flava Klapálek 1916, K. neotropica (Jacobson and Bianchi 1905) (including its new junior synonym K. petersorum Froehlich 1996), Kempnyia sp., and Macrogynoplax veneranda Froehlich 1984. COI sequences were obtained for 11 species, five of which had nymphs associated with adults. Among the five associated nymphs, the nymph of A. tupi is described here. The results of this study indicate that the color of adult teneral specimens differs from that of mature specimens. Given this, the synonym of K. neotropica and K. petersorum was proposed since these species have high morphological and molecular similarities and differ only in color patterns. In addition, the previous record of A. petersi Froehlich 2002 from the Paranapiacaba Mountains was invalidated since it was considered a teneral specimen of A. flintorum. These results suggest that the development of an integrative taxonomy is essential to continue advancing the study of Perlidae diversity in South America.

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Integrative taxonomy refutes a species hypothesis: The asymmetric hybrid origin of Arsapnia arapahoe (Plecoptera, Capniidae).

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