Multilocus genetic analyses differentiate between widespread and spatially restricted cryptic species in a model ascidian

Abstract

Elucidating the factors that shape species distributions has long been a fundamental goal in ecology and evolutionary biology. In spite of significant theoretical advancements, empirical studies of range limits have lagged behind. Specifically, little is known about how the attributes that allow species to expand their ranges and become widespread vary across phylogenies. Here, we studied the ascidian Botryllus schlosseri, a worldwide invasive species that is also characterized by marked genetic subdivision. Our study includes phylogenetic and population genetic data based on mitochondrial and nuclear genes, as well as polymorphic microsatellites for B. schlosseri colonies sampled from the southern and northern coasts of Europe and the eastern and western coasts of North America. We demonstrate that this well-known model organism comprises three highly divergent and probably reproductively isolated cryptic species (A, D and E), with two more (B and C) being suggested by data retrieved from GenBank. Among these, species A, recovered in all of the surveyed regions, is by far the most common and widespread. By contrast, species B-E, occurring mostly in sites from northern Europe, are considerably more geographically restricted. These findings, along with inferences made on transport opportunity, suggest that divergent evolutionary histories promoted differences in invasive potential between B. schlosseri sibling species, indicating that attributes that facilitate dramatic shifts in range limits can evolve more easily and frequently than previously thought. We propose environmental disturbance as a selective force that could have shaped the evolution of invasiveness in the B. schlosseri complex.

Figure 1.

Distribution of sampling locations and phylogenetic clades for B. schlosseri on the (a) west and (b) east coasts of North America, and (c) in Europe. Site IDs are defined in table 1. Filled circles, clade A; filled triangles, clade D; open squares, clade E.

Figure 2.

Neighbour-joining (NJ) tree based on mitochondrial cytochrome c oxidase I (COI) haplotypes and nuclear 18S rRNA sequences. Numbers at phylogenetic nodes indicate NJ bootstrap support and Bayesian inference posterior probabilities. The number of samples showing a given haplotype is presented in brackets.

Figure 3.

Factorial correspondence analysis of clade A microsatellite data (considering 10 loci) showing genetic similarities of sampled individuals (derived from allele frequencies). Grey circles, southern Europe; black circles, northern Europe; crossed circles, eastern North America; white circles, western North America.

Figure 4.

Bayesian clustering of microsatellite data obtained for all samples (considering seven loci). Each individual is represented by a thin vertical line partitioned into K = 3 coloured segments (clade A, red; clade D, blue; clade E, yellow) representing the individual's estimated admixture coefficient. Sampling sites are separated by black lines. Site IDs are defined in table 1.