Population genomics of the introduced and cultivated Pacific kelp Undaria pinnatifida: Marinas—not farms—drive regional connectivity and establishment in natural rocky reefs

Abstract

Ports and farms are well‐known primary introduction hot spots for marine non‐indigenous species (NIS). The extent to which these anthropogenic habitats are sustainable sources of propagules and influence the evolution of NIS in natural habitats was examined in the edible seaweed Undaria pinnatifida, native to Asia and introduced to Europe in the 1970s. Following its deliberate introduction 40 years ago along the French coast of the English Channel, this kelp is now found in three contrasting habitat types: farms, marinas and natural rocky reefs. In the light of the continuous spread of this NIS, it is imperative to better understand the processes behind its sustainable establishment in the wild. In addition, developing effective management plans to curtail the spread of U. pinnatifida requires determining how the three types of populations interact with one another. In addition to an analysis using microsatellite markers, we developed, for the first time in a kelp, a ddRAD‐sequencing technique to genotype 738 individuals sampled in 11 rocky reefs, 12 marinas, and two farms located along ca. 1,000 km of coastline. As expected, the RAD‐seq panel showed more power than the microsatellite panel for identifying fine‐grained patterns. However, both panels demonstrated habitat‐specific properties of the study populations. In particular, farms displayed very low genetic diversity and no inbreeding conversely to populations in marinas and natural rocky reefs. In addition, strong, but chaotic regional genetic structure, was revealed, consistent with human‐mediated dispersal (e.g., leisure boating). We also uncovered a tight relationship between populations in rocky reefs and those in nearby marinas, but not with nearby farms, suggesting spillover from marinas into the wild. At last, a temporal survey spanning 20 generations showed that wild populations are now self‐sustaining, albeit there was no evidence for local adaptation to any of the three habitats. These findings highlight that limiting the spread of U. pinnatifida requires efficient management policies that also target marinas.

Habitat type drives the distribution of non‐indigenous species in fouling communities regardless of associated maritime traffic

“…In seemingly “open” marine systems, the relative influence of both types of dispersal is however expected to differ according to pelagic dispersal duration, with a putative larger influence of human‐mediated dispersal for species characterized by short‐lived dispersal stage. This expectation has been supported by genetic studies of short dispersers, such as the tunicate Ciona intestinalis (Hudson, Viard, Roby, & Rius, ) or the Pacific kelp Undaria pinnatifida (Guzinski, Ballenghien, Daguin‐Thiébaut, Lévêque, & Viard, ): in marinas, these species display chaotic genetic structure at regional scale, which is best explained by the role of shipping than natural dispersal. The influence of human‐mediated dispersal may however be less important in marine invertebrates displaying larval stage lasting typically 3–5 weeks in the water column (e.g.…”

Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels

“…Given the presence of marinas in the vicinity of the large studied ports and their colonisation by dock mussels, they constitute a possible way of secondary expansion at a regional scale. Indeed, marinas and associated activities, for example leisure boating, have been shown to contribute to regional NIS expansion (Clarke Murray, Pakhomov, & Therriault, 2011) and create chaotic genetic structure in both native and non-native species inhabiting these artificial habitats (Guzinski, Ballenghien, Daguin-Thiébaut, Lévêque, & Viard, 2018;Hudson, Viard, Roby, & Rius, 2016). For now, in the Bay of Brest, only the marinas close to the large port contained dock mussels.…”

A genome‐wide investigation of the worldwide invader Sargassum muticum shows high success albeit (almost) no genetic diversity

“…However, the most striking result was the absence of genetic diversity across 14 microsatellite markers over more than 1,000 samples from both introduction ranges ( Figure 1). This lack of diversity contrasts sharply with other seaweed cases: for instance, a recent study by Guzinski et al (2018) showed that a dozen microsatellites provided roughly similar results as several thousand SNPs obtained from ddRAD sequencing to analyze the connectivity and adaptation processes in the introduced seaweed U. pinnatifida, at a regional scale. So far, introduced populations of sexually reproducing marine invaders have never been shown to be monomorphic at microsatellites or similar type of highly variable markers.…”