Genetic identification of source and likely vector of a widespread marine invader

Abstract

The identification of native sources and vectors of introduced species informs their ecological and evolutionary history and may guide policies that seek to prevent future introductions. Population genetics provides a powerful set of tools to identify origins and vectors. However, these tools can mislead when the native range is poorly sampled or few molecular markers are used. Here, we traced the introduction of the Asian seaweed Gracilaria vermiculophylla (Rhodophyta) into estuaries in coastal western North America, the eastern United States, Europe, and northwestern Africa by genotyping more than 2,500 thalli from 37 native and 53 non‐native sites at mitochondrial cox1 and 10 nuclear microsatellite loci. Overall, greater than 90% of introduced thalli had a genetic signature similar to thalli sampled from the coastline of northeastern Japan, strongly indicating this region served as the principal source of the invasion. Notably, northeastern Japan exported the vast majority of the oyster Crassostrea gigas during the 20th century. The preponderance of evidence suggests G. vermiculophylla may have been inadvertently introduced with C. gigas shipments and that northeastern Japan is a common source region for estuarine invaders. Each invaded coastline reflected a complex mix of direct introductions from Japan and secondary introductions from other invaded coastlines. The spread of G. vermiculophylla along each coastline was likely facilitated by aquaculture, fishing, and boating activities. Our ability to document a source region was enabled by a robust sampling of locations and loci that previous studies lacked and strong phylogeographic structure along native coastlines.

Nonnative Gracilaria vermiculophylla tetrasporophytes are more difficult to debranch and are less nutritious than gametophytes

“…, Krueger‐Hadfield et al. ,, ). These data will shed light on the invasion ecology of important ecosystem engineers, and advance our understanding of life cycle evolution, and the maintenance of life cycle diversity.…”

“…, Krueger‐Hadfield et al. ). It is a novel ecosystem engineer in habitats that were historically devoid of macroalgae (Byers et al.…”

“…), and in ~40% of the nonnative sites surveyed, no gametophytic thalli have been found along sampled transects (Krueger‐Hadfield et al. , ). While haploid‐dominated populations in other Gracilaria species have been documented (Kain and Destombe , Arakaki et al.…”

“…), we have not yet encountered a gametophyte‐dominated population in the non‐native range of Gracilaria vermiculophylla (Krueger‐Hadfield et al. , ). Thus, the trend of tetrasporophytic bias in the native range coupled with dominance in nonnative soft‐sediment habitats suggest, at a minimum, that tetrasporophytes and gametophytes differ in their phenotypes and ecological performance (Kain and Destombe , Guillemin et al.…”

“…Gracilaria vermiculophylla (Gracilariales) is native to the northwest Pacific, and has invaded temperate estuaries along the coastlines of North America, Europe, and northern Africa (Bellorin et al 2004, Rueness 2005, Guillemin et al 2008a, Saunders 2009, Kim et al 2010, Krueger-Hadfield et al 2017. It is a novel ecosystem engineer in habitats that were historically devoid of macroalgae (Byers et al 2012), with both positive (e.g., Thomsen and McGlathery 2005, Thomsen 2010, Kollars et al 2016 and negative ecological impacts (e.g., Freshwater et al 2006).…”