The Story of a Hitchhiker: Population Genetic Patterns in the Invasive Barnacle Balanus(Amphibalanus) improvisus Darwin 1854

Abstract

Understanding the ecological and evolutionary forces that determine the genetic structure and spread of invasive species is a key component of invasion biology. The bay barnacle, Balanus improvisus (= Amphibalanus improvisus), is one of the most successful aquatic invaders worldwide, and is characterised by broad environmental tolerance. Although the species can spread through natural larval dispersal, human-mediated transport through (primarily) shipping has almost certainly contributed to the current global distribution of this species. Despite its worldwide distribution, little is known about the phylogeography of this species. Here, we characterize the population genetic structure and model dispersal dynamics of the barnacle B. improvisus, and describe how human-mediated spreading via shipping as well as natural larval dispersal may have contributed to observed genetic variation. We used both mitochondrial DNA (cytochrome c oxidase subunit I: COI) and nuclear microsatellites to characterize the genetic structure in 14 populations of B. improvisus on a global and regional scale (Baltic Sea). Genetic diversity was high in most populations, and many haplotypes were shared among populations on a global scale, indicating that long-distance dispersal (presumably through shipping and other anthropogenic activities) has played an important role in shaping the population genetic structure of this cosmopolitan species. We could not clearly confirm prior claims that B. improvisus originates from the western margins of the Atlantic coasts; although there were indications that Argentina could be part of a native region. In addition to dispersal via shipping, we show that natural larval dispersal may play an important role for further colonisation following initial introduction.

Fig 1. Distribution of haplotypes in the different populations of B. improvisus.

The twelve most common haplotypes (represented by five or more individuals) are colour-coded and the “white proportion” contains all the haplotypes represented by five or less individuals including unique haplotypes.

Fig 2. A minimum spanning haplotype network based on a 694 bp fragment of the mtDNA COI gene in B. improvisus.

Each node represents one mutational step and the size of each circle represents the frequency of a haplotype. The pie chart colours represent different geographical groupings of populations; PU = Pacific US, AU = Atlantic US (North Carolina and Chesapeake Bay combined), AR = Argentina, FR = France, BS = Baltic South (including Kiel, Torhamn, Estonia and Saltö), BN = Baltic North (Öregrund and Umeå), CA = Central Asia (Caspian Sea and Black Sea) and JP = Japan. Small empty circles (nodes) represent non-sampled haplotypes.

Fig 3. Mismatch distributions based on COI sequences from B. improvisus populations.

Observed mismatch distribution (bars) and expected mismatch distributions under the sudden expansion model (solid line) of mtDNA COI sequences for each population. D = Tajima’s D, F_S = Fu’s F_S, R = raggedness value. Significance is presented as *: P = 0.01–0.05, **: P < 0.01. The populations are sorted according to the pattern of mismatch distribution, with populations displaying more diverged haplotypes (2–4 mismatches) to the left, and populations with less differentiated haplotypes (1–2 mismatches) to the right.

Fig 4. Non-metric multidimensional scaling plot (MDS) based on Slatkin’s linearized distances among populations of B. improvisus.

A) MDS based on mtDNA (Φ_ST): stress: 0.064; B) MDS based on microsatellites (F_ST): data including all four loci with null allele correction, stress: 0.11 (stress values over 0.2 suggest that the precision in representing the relationships among populations is limited).

Fig 5. Correlating pairwise genetic distances between B. improvisus populations to geographical distance and oceanographic connectivity.

Pairwise genetic distance (Φ_ST, COI) for populations of B. improvisus in the Baltic Sea plotted as a function of (a) closest geographical shipping distance (km) (Mantel test: R = 0.46, p = 0.075); (b) minimum oceanographic connectivity between sampling sites; (c) standardised and null allele corrected pairwise genetic distance ((F_ST/1-F_ST) in microsatellites plotted as a function of minimum oceanographic connectivity between sampling sites.