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Phylogeography and population genetics of introduced Silver Carp (Hypophthalmichthys molitrix) and Bighead Carp (H. nobilis) in North America

Abstract

The success of a biological invasion and the ability to control an invader may partially depend on the genetic diversity of the invasive species and the amount of dispersal and gene flow occurring throughout its introduced range. Here, we used nuclear microsatellites to analyze genetic diversity and structure and whole mitogenomic sequences to analyze the phylogeography of Silver Carp (SC; Hypophthalmichthys molitrix) and Bighead Carp (BHC; H. nobilis) across their North American ranges. Our objectives were to assess: (1) the number of mitochondrial haplotypes that were introduced and how they are distributed in North America, which may provide insight into the history of the invasion, (2) how genetic diversity compares between the native Asian and introduced North American populations, (3) how genetic variation is structured across the North American ranges of SC and BHC as well as between the two species, and (4) whether patterns of genetic diversity and structure are likely to affect success of environmental DNA programs for monitoring these species. In both species, we found relatively few mitochondrial haplotypes, and most were present throughout the range. For both SC and BHC, unique haplotypes were found only in a portion of the species’ range, possibly indicating the location of additional, more recent introductions. In both species, genetic diversity was moderately lower in North American populations (i.e., 75–90% of that found in Asian populations), but genetic diversity still remained high. We found very little population genetic structure, consistent with a rapidly spreading invasive species, and did not find evidence of cryptic interspecific hybrids. The markers developed for eDNA monitoring will be effective for detecting the majority of individuals of these species in North America. The relatively high level of genetic variation and lack of population structure of SC and BHC in North America indicate that genetic diversity likely will not limit their persistence and that high connectivity will likely complicate efforts to control these invasive species.

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Acknowledgements

We thank Kelly Baerwaldt for overseeing, representing, and supporting the greater eDNA Calibration Study, of which the research presented here was one component; James Lamer, Jack Kilgore, Steven George, Alan Katzmeyer, Sifa Li, Duane Chapman, Guoqing Lu for coordinating sample collection or for providing tissue samples; Michael Jung (ERDC), Karen Bascom (ERDC), Matthew Carr (ERDC), Shannon Julian (USFWS) and Neihl Williamson (USFWS) for laboratory support; Burgund Bassüner (MOBOT) for assisting with preparation of the map of the collection sites; Denise Lindsay and Xin Guan for logistical support. Funding for this project was provided to MB and RFL through the eDNA calibration project by the Great Lakes Restoration Initiative. The views, findings, and conclusions expressed in this manuscript are those of the author’s and do not reflect the official policy or position of the U. S. Fish and Wildlife Service, the Department of the Army, Department of Defense, or the U.S. Government. The use of trade, product, or firm names in this paper is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Correspondence to Christine E. Edwards.

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All sample collection followed guidelines provided by the American Society for Ichthyologists and Herpetologists’ (ASIH) Guidelines for the Use of Fishes in Research (American Fisheries Society 2004). For individuals within the native range, a small piece of caudal fin from each fish was clipped and then animals were released. Within the introduced range, it is illegal to release live Silver Carp and Bighead Carp according to the provisions mandated by the Lacey Act and the Asian Carp Prevention and Control Act; individuals were therefore rapidly euthanized in order to minimize stress and suffering. Silver and Bighead carp were collected from the middle and lower Mississippi under authorities granted by state scientific collecting permits for Arkansas (#053120121), Louisiana (#118), Mississippi (#0827121) and the Illinois River and Chicago Area Waterway System by the Illinois Department of Natural Resources under statutory authority granted under Illinois Fish and Wildlife Statutes 515 ILCS 5/20– 100 and 520 ILCS 5/3.22.

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10530_2017_1484_MOESM1_ESM.jpg

Fig. S1. Unrooted neighbor-joining phylogram of Nei’s (1978) genetic distances based on microsatellite data for Silver Carp (A) and Bighead Carp (B). (JPEG 25 kb)

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Farrington, H.L., Edwards, C.E., Bartron, M. et al. Phylogeography and population genetics of introduced Silver Carp (Hypophthalmichthys molitrix) and Bighead Carp (H. nobilis) in North America. Biol Invasions 19, 2789–2811 (2017). https://doi.org/10.1007/s10530-017-1484-3

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Keywords

  • Silver Carp
  • Bighead Carp
  • Invasive species
  • Mitogenome
  • Microsatellites
  • Genetic diversity
  • Genetic structure