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Invasion Genetics of the Silver Carp (Hypophthalmichthys Molitrix) Across North America: Differentiation of Fronts, Introgressio

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Invasion Genetics of the Silver Carp (Hypophthalmichthys Molitrix) Across North America: Differentiation of Fronts, Introgressio bioRxiv preprint doi: https://doi.org/10.1101/392704; this version posted August 15, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 1 Invasion genetics of the silver carp (Hypophthalmichthys molitrix) across 2 North America: Differentiation of fronts, introgression, and eDNA detection 3 August 9 2018 4 5 Carol A. Stepiena,b*, Anna E. Elza, and Matthew R. Snydera,b 6 7 aNOAA Pacific Marine Environmental Laboratory, Genetics and Genomics Group (G3), 8 7600 Sand Point Way NE, Seattle, WA, 98115, USA 9 10 bDepartment of Environmental Sciences, Genetics and Genomics Group, University of Toledo, 11 OH, 43606, USA 12 13 *Corresponding Author: [email protected], [email protected] 14 15 Short Title: Silver carp invasion genetics 1 bioRxiv preprint doi: https://doi.org/10.1101/392704; this version posted August 15, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 16 Abstract 17 The invasive silver carp Hypophthalmichthys molitrix escaped from southern U.S. aquaculture 18 during the 1970s to spread throughout the Mississippi River basin and steadily moved northward, 19 now reaching the threshold of the Laurentian Great Lakes. The silver carp is native to eastern 20 Asia and is a large, prolific filter-feeder that decreases food availability for fisheries. The present 21 study evaluates its population genetic variability and differentiation across the introduced range 22 using 10 nuclear DNA microsatellite loci, sequences of two mitochondrial genes (cytochrome b 23 and cytochrome c oxidase subunit 1), and a nuclear gene (ribosomal protein S7 gene intron 1). 24 Populations are analyzed from two invasion fronts threatening the Great Lakes (the Illinois River 25 outside Lake Michigan and the Wabash River, leading into the Maumee River and western Lake 26 Erie), established areas in the southern and central Mississippi River, and a later Missouri River 27 colonization. Results discern considerable genetic diversity and some significant population 28 differentiation, with greater mtDNA haplotype diversity and unique microsatellite alleles 29 characterizing the southern populations. Invasion fronts significantly differ, diverging from the 30 southern Mississippi River population. About 3% of individuals contain a unique and very 31 divergent mtDNA haplotype (primarily the southerly populations and the Wabash River), which 32 may stem from historic introgression in Asia with female largescale silver carp H. harmandi. 33 Nuclear microsatellites and S7 sequences of the introgressed individuals do not significantly 34 differ from silver carp. MtDNA variation is used in a high-throughput sequence assay that 35 identifies and distinguishes invasive carp species and their population haplotypes (including H. 36 molitrix and H. harmandi) at all life stages, in application to environmental (e)DNA water and 37 plankton samples. We discerned silver and bighead carp eDNA from four bait and pond stores in 38 the Great Lakes watershed, indicating that release from retailers comprises another likely vector. 39 Our findings provide key baseline population genetic data for understanding and tracing the 40 invasion’s progression, facilitating detection, and evaluating future trajectory and adaptive 41 success. 42 43 2 bioRxiv preprint doi: https://doi.org/10.1101/392704; this version posted August 15, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 44 Introduction 45 Discerning the population genetic trajectories of nonindigenous species invasions can enhance 46 our overall understanding of the evolutionary adaptations and changing ecological community 47 dynamics governing today’s ecosystems [1–3]. Establishments by invasive species comprise 48 accidental experiments that ground-truth evolutionary and ecological theory with reality [4–6]. 49 The genetic variation of invasive populations often affects their relative success and persistence 50 in new habitats, including colonizing, reproducing, spreading, and overcoming biotic resistance 51 [2, 7, 8]. 52 53 Invasion genetics 54 55 Invasion biology theory predicts that many introduced species would be characterized by low 56 genetic diversity due to founder effect, which is believed to limit their adaptive potential (9 –11). 57 Countering this, large numbers of introduced propagules and multiple introduction events and 58 sources may enhance the genetic diversity of invasions, with some actually possessing higher 59 levels than found in native regions [12–14]. For example, genetic studies of North American 60 Laurentian Great Lakes invasions resulting from ballast water introductions of the Eurasian zebra 61 mussel Dreissena polymorpha (Pallas, 1771), quagga mussel D. rostriformis (Deshayes, 1838) 62 [15, 16], and round goby Neogobius melanostomus (Pallas, 1814) [5, 17–19], all discerned 63 relatively high genetic diversities, along with significant population differentiation across their 64 introduced ranges. These results were attributed to large numbers of introduced propagules 65 stemming from multiple introduction events, which traced to several Eurasian sources. Such 66 cases of high genetic variability are believed to enhance the adaptive potential of invasions (see 67 [11]). 68 Populations at the expansion fronts of an invasion front frequently possess less genetic 69 variability than those at the core of the invasion, which is termed the “leading edge” hypothesis 70 [20, 21]. The phenotypes of individuals at these front populations are postulated to be adapted 71 for dispersal and high reproductive output [22], where they experience low population density, 72 and may benefit from greater resource availability and less intraspecific competition, 73 enhancing reproductive success [23, 24]. These processes may lead to genetic differences in 74 expansion fronts versus longer-established populations, which may result from drift and/or 3 bioRxiv preprint doi: https://doi.org/10.1101/392704; this version posted August 15, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 75 selection. However, documentation of their comparative genetics across the spatial and 76 temporal course of invasions are relatively rare in the literature [22]. 77 Sometimes closely related invasive species, which may interact competitively, are 78 introduced together or in close succession, as occurred in the Laurentian Great Lakes for the 79 zebra and quagga mussels [25–27], with the latter overtaking the former in many areas [28, 29]. 80 Another case of simultaneous introduction by related species include the Eurasian round and 81 tubenose Proterorhinus semilunaris gobies [30], with the former continuing to be much more 82 numerous and widespread in the Great Lakes [31]. In the 1960s and 1970s, the closely related 83 east-Asian silver Hypophthalmichthys molitrix (Valenciennes 1884) and bighead H. nobilis 84 (Richardson 1845) carps both were intentionally introduced to the southern U.S. to control algae 85 [32]. The two species are known to hybridize [33, 34], which may increase their success via 86 “hybrid vigor”. Silver and bighead carps were raised at six state, federal, and private facilities in 87 Arkansas during the 1970s, and had been stocked into several municipal sewage lagoons [35]. 88 They escaped in the 1970s and became established in the Mississippi River basin [32], spreading 89 into the upper Mississippi River system [36]. The two species now are near the Great Lakes in 90 the Illinois River system outside of Lake Michigan in the vicinity of Chicago IL, with growing 91 concern that they will enter and become established in the Great Lakes [37, 38]. 92 The Great Lakes already constitute one of the world’s most heavily invaded aquatic 93 ecosystems, harboring over 186 reported invasive species, with the most significant ecological 94 impacts caused by the invasions of the sea lamprey Petromyzon marinus, common carp Cyprinus 95 carpo, zebra and quagga mussels, round goby, spiny waterflea, and rusty crayfish Orconectes 96 rusticus. Ecologists have theorized that such a long history of established invasions is believed to 97 increase the chances of success by subsequent invaders [39]. This may pave the way to success 98 of the silver and bighead carps, with the grass carp Ctenopharyngodon idella now recently 99 established in Lake Erie [40]. 100 Accidental releases from aquaculture operations are a primary vector for introductions of 101 exotic species [41], as led to the establishment of wild populations of silver and bighead carps in 102 North America [32]. Other cases include the widespread escapes and establishments by tilapia 103 (Oreochromis spp., Sarotherodon spp., and Tilapia spp.) [42], and cultured bivalves, including 104 the Pacific oyster (Crassostrea gigas) in North America and Europe, and the Mediterranean
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