"Nested" cryptic diversity in a widespread marine ecosystem engineer: a challenge for detecting biological invasions

Abstract

BackgroundEcosystem engineers facilitate habitat formation and enhance biodiversity, but when they become invasive, they present a critical threat to native communities because they can drastically alter the receiving habitat. Management of such species thus needs to be a priority, but the poorly resolved taxonomy of many ecosystem engineers represents a major obstacle to correctly identifying them as being either native or introduced. We address this dilemma by studying the sea squirt Pyura stolonifera, an important ecosystem engineer that dominates coastal communities particularly in the southern hemisphere. Using DNA sequence data from four independently evolving loci, we aimed to determine levels of cryptic diversity, the invasive or native status of each regional population, and the most appropriate sampling design for identifying the geographic ranges of each evolutionary unit.ResultsExtensive sampling in Africa, Australasia and South America revealed the existence of "nested" levels of cryptic diversity, in which at least five distinct species can be further subdivided into smaller-scale genetic lineages. The ranges of several evolutionary units are limited by well-documented biogeographic disjunctions. Evidence for both cryptic native diversity and the existence of invasive populations allows us to considerably refine our view of the native versus introduced status of the evolutionary units within Pyura stolonifera in the different coastal communities they dominate.ConclusionsThis study illustrates the degree of taxonomic complexity that can exist within widespread species for which there is little taxonomic expertise, and it highlights the challenges involved in distinguishing between indigenous and introduced populations. The fact that multiple genetic lineages can be native to a single geographic region indicates that it is imperative to obtain samples from as many different habitat types and biotic zones as possible when attempting to identify the source region of a putative invader. "Nested" cryptic diversity, and the difficulties in correctly identifying invasive species that arise from it, represent a major challenge for managing biodiversity.

Genetic and morphological diversification in gastropods of the Baicaliidae family

“…The ATP synthase α subunit intron, along with the mitochondrial molecular markers, was already used earlier as a phylogenetic marker in several studies (Freya and Vermeij, 2008;Keever et al, 2009;Hedtke et al, 2011;Teske et al, 2011;Feher et al, 2012;Puritz et al, 2012).…”

Globally intertwined evolutionary history of giant barrel sponges

“…Usually, there is a general conformity between phylogeography and biogeography in marine animal groups, which suggests that geographic isolation is a starting point for divergences between species (Teske et al 2011;Bowen et al 2016). Most global marine species complexes are so-called 'sibling species complexes' that developed simultaneously in different ocean basins, potentially followed by cryptic invasions (Schwaninger 2008;Geller et al 2010).…”

“…Genetic markers have become increasingly important tools to identify divergent cryptic species and have forced the rejection of the long-believed assumption of cosmopolitan distribution of certain species (Boury-Esnault et al 1992;Knowlton 1993;Klautau et al 1999). Molecular techniques have also helped to reconstruct the distributional patterns of invasive species, which have become major drivers of ecosystem change due to the increase in global shipping (Concepcion et al 2010;Teske et al 2011). Most studies that have focused on the distribution and evolution of marine species cover small spatial scales and become more useful when they are compared to more wide-ranging studies (Briggs and Bowen 2013;Cowman and Bellwood 2013a).…”

Population genetic analyses are consistent with the introduction of Ceramium secundatum (Ceramiaceae, Rhodophyta) to Narragansett Bay, Rhode Island, USA

“…These negative impacts that transpire when introduced species become invasive create irreversible modifications to native communities (Teske et al. 2011). Cryptic introductions are particularly problematic because of the challenges in detecting, quantifying and monitoring changes within the ecosystem (Geller et al.…”