Genetic and morphological discrimination of three species of ninespined stickleback Pungitius spp. (Teleostei, Gasterosteidae) in France with the revalidation of Pungitius vulgaris (Mauduyt, 1848)

Abstract

The taxonomy of French ninespined sticklebacks (Pungitius spp.) has long been controversial. To clarify the taxonomy in this group, we use mitochondrial (COI) and nuclear (RNF213) sequence markers, as well as morphological data. In France, both genetic markers discriminate three evolutionary lineages. Morphological analysis on fresh and type specimens supports the different lineages and the existence of three species in France. Pungitius pungitius, occurring in the North of France and Rhone basin, is characterized by specimens longer than 35 mm SL, by a flat head with a straight or slightly concave snout, typically 9–10 dorsal spines, 10–11 dorsal soft rays, 9–10 anal soft rays, 0–12 scutes on the caudal peduncle with a keel reaching the last anal‐fin ray, longer pelvic fin, post‐dorsal and caudal peduncle lengths, and a slim caudal peduncle (caudal peduncle depth/length 11.8%–21.9%). Pungitius laevis, occurring in France, in the English Channel basins and Loire drainage, differs from the other species by a head rounded with concave snout in specimens longer than 35 mm SL, accentuating the impression of fleshy lips, 0–4 scutes on the caudal peduncle and a higher caudal peduncle depth/length ratio (15.7%–34.5%). Finally, Pungitius vulgaris, endemic to the Vienne River and rivers of south‐western France as far north as the Garonne estuary, is differentiated by a rounded head with a straight or slightly convex snout, the absence of scutes on the caudal peduncle and by having 11 pectoral‐fin rays. Our data confirm the existence of a hybridization zone in the North of France between P. pungitius and P. laevis. As a result, Pungitius lotharingus is invalid, as it was described based on hybrid specimens. A lectotype for P. laevis was designated because the syntypes included hybrids. This revision provides new perspectives for evolutionary biology studies and will have consequences for Pungitius conservation in France.

A phylogenomic perspective on diversity, hybridization and evolutionary affinities in the stickleback genusPungitius

“…The clearest case is the suggested transfer of the mitogenome from the Western European lineage of P. pungitius to P. laevis . As the two species are parapatric and co‐occur in several areas (Denys et al, ; Kottelat & Freyhof ; Wang et al, ), this scenario is biologically plausible. Theoretically, because the two species are also very closely related and diverged only 3.33 Mya, incomplete lineage sorting could also account for the fact that some individuals of P. laevis share the same mitochondrial haplotype with P. pungitius .…”

“…Also, divergence among the three distinct P. laevis lineages (see also: Wang et al, ) was high (1.1%–1.8%), suggesting that P. laevis might actually contain more than one distinct species. However, according to the 3% demarcation criterion above, the different P. laevis lineages would still perhaps best be considered as a single species (but see: Denys et al, ).…”

“…However, according to the 3% demarcation criterion above, the different P. laevis lineages would still perhaps best be considered as a single species (but see: Denys et al, 2018).…”

“…Third, current understanding of phylogenetic relationships in the Pungitius species complex resides heavily on mitochondrial DNA sequences (e.g., Bae & Suk, 2015;Takahashi & Goto, 2001;Teacher, Shikano, Karjalainen, & Merilä, 2011;Wang et al, 2015), and only a few studies-all based on either limited geographical or taxon sampling-have utilized nuclear genetic information (Aldenhoven, Miller, Corneli, & Shapiro, 2010;Bae & Suk, 2015;Haglund et al, 1992;Natri, Merilä, & Shikano, 2019;Shikano, Ramadevi, Shimada, & Merilä, 2010;Takahashi et al, 2016;Takata, Goto, & Yamazaki, 1987b;Wang, Shikano, Persat, & Merilä, 2017). Phylogenetic studies based on a large number of nuclear loci are motivated by the well-known limitations of phylogenetic and phylogeographical inferences based on mitochondrial information (e.g., Ballard & Whitlock, 2004;Hey & Machado, 2003;Toews & Brelsford, 2012), as well as by the evidence for weak post-zygotic isolation (Kobayashi, 1959;Takahashi, Nagai, & Goto, 2005;Tsuruta & Goto, 2006;Ziuganov & Gomeluk, 1985), and hybridization in this genus (Denys et al, 2018;Niwa, 1987;Takahashi et al, 2016;Takahashi & Takata, 2000;Wang et al, 2017;Natri et al, 2019).…”

Alien Fish Species in France with Emphasis on the Recent Invasion of Gobies

“…Traditionally about 80 species were recognized [34], yet with the advent of the DNA barcoding and integrative taxonomy [44] several taxonomic revisions have been done: some new species have been described [45][46][47], others have been invalidated [48]. For instance, it was thought that the Northern pike (Esox Lucius) was the only species present in Europe, but recent integrative analyses based on both morphological and molecular characters concluded that three species are actually present in France, the Northern pike (which is the most common), E. aquitanicus (from the Charente to the Adour drainages), and E. cisalpinus (mostly in the Lake Geneva).…”