Hybridization and adaptive introgression in a marine invasive species in native habitats

Abstract

Hybridization of distinct populations or species is an important evolutionary driving force. For invasive species, hybridization can enhance their competitive advantage as a source of adaptive novelty by introgression of selectively favored alleles. Using single-nucleotide polymorphism (SNP) microarrays we assess genetic diversity and population structure in the invasive ctenophore Mnemiopsis leidyi in native habitats. Hybrids are present at the distribution border of two lineages, especially in highly fluctuating environments including very low salinities, while hybrids occur at lower frequency in stable high-saline habitats. Analyses of hybridization status suggest that hybrids thriving in variable environments are selected for, while they are selected against in stable habitats. Translocation of hybrids might accelerate invasion success in non-native habitats. This could be especially relevant for M. leidyi as low salinity limits its invasion range in western Eurasia. Although hybridization status is currently disregarded, it could determine high-risk areas where ballast water exchange should be prevented.

Keywords: Environmental science; Evolutionary biology; Nature conservation.

Graphical abstract

Figure 1

Mnemiopsis leidyi sampling locations, USA east coast (2018/2020), and hybrid population classification (A) Northern populations (blue triangle up) with stations (WH = Woods Hole, MA; SA = Sandwich, MA; EP = Long Island Sound, Esker Point, CT and Narraganset Bay, RI with FA = Fort Adams, FW = Fort Wetherill, GC = Greenwich Cove), hybrid populations (pink diamond) with Chesapeake Bay (GP = Gloucester Point, VA) and Atlantic coast (WA = Wachapreague, VA). Southern population (red triangle down) with MI = Miami, FL; Cape Hatteras indicates population border (hatched line). (B) Hybrid populations with proportion of pure northern (blue), F₂/F_x-hybrids (green), 1^st generation (yellow) and 2^nd generation (orange) backcrosses inside and outside of Chesapeake Bay, 2018.

Figure 2

Principal component analysis (PCA) for Mnemiopsis leidyi populations along the USA east coast (2018/2020) Northern populations (blue triangles): WH = Woods Hole, MA; SA = Sandwich, MA; EP = Long Island Sound, Esker Point, CT and Narraganset Bay, RI with FA = Fort Adams, FW = Fort Wetherill, GC = Greenwich Cove; hybrid populations (pink diamonds): Chesapeake Bay (GP = Gloucester Point, VA) and Atlantic coast (WA = Wachapreague, VA); and southern population (red downward triangles): MI = Miami, Florida).

Figure 3

Admixture analysis visualized by STRUCTURE plots of Mnemiopsis leidyi sampled along the US east coast Individuals were assigned on the basis of the most likely K, in this case (K = 2). Locations as outlined in Figure 1 (SA = Sandwich, MA; WH = Woods Hole, MA; FA = Fort Adams, RI; FW = Fort Wetherill, RI; GC = Greenwich Cove, RI; EP = Esker Point, CT; WA = Wachapreague, VA; GP = Gloucester Point, Chesapeake Bay, VA; MI = Miami, FL).

Figure 4

Average yearly surface salinity of Chesapeake Bay (1985–2018) with selected M. leidyi observations from literature Red dots from (a) Purcell and Decker (2005), (b) Condon and Steinberg (2008), (c) Bi et al. (2013), (d) Bayha et al. (2015), (e) Verwimp et al. (2019), (f) Slater et al. (2020), (g) this study; blue dots from Purcell et al. (2001); pink dots from Chesapeake Bay program—sourced 20.5.2023. Schematic map sourced and modified from Chesapeake Bay Program along with presence of M. leidyi data (www.chesapeakebay.net), sampling locations approximated.

Figure 5

Schematic drawing of F₁/F₂ hybrids and 1^st/2^nd generation backcrosses Admixture analysis for all simulated data using STRUCTURE. Individuals were assigned on the basis of the most likely K, in this case (K = 2). A total of 12 categories were simulated: pure northern lineage (WH), pure southern lineage (MI), F₁ hybrid, F₂ hybrid, first-generation backcross northern × F₁ (bWH), first-generation backcross southern × F₁ (bMI) and second-generation backcrosses (bWH × WH, bWH × MI, bWH × F₁, bMI × MI, bMI × WH and bMI × F₁).