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Open Access Highly Accessed Research article

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

Peter R Teske1234*, Marc Rius56, Christopher D McQuaid3, Craig A Styan78, Maxine P Piggott9, Saïd Benhissoune10, Claudio Fuentes-Grünewald11, Kathy Walls12, Mike Page13, Catherine RM Attard2, Georgina M Cooke2, Claire F McClusky7, Sam C Banks9, Nigel P Barker4 and Luciano B Beheregaray12

Author Affiliations

1 Molecular Ecology Laboratory, School of Biological Sciences, Flinders University, Adelaide, SA 5001, Australia

2 Molecular Ecology Laboratory, Department of Biological Sciences, Macquarie University, Sydney 2109, Australia

3 Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa

4 Molecular Ecology and Systematics Group, Rhodes University, Grahamstown 6140, South Africa

5 Centre for Invasion Biology, Zoology Department, University of Cape Town, Rondebosch 7701, South Africa

6 Current Address: Department of Evolution and Ecology, University of California, One Shields Avenue, Davis, California 95616, USA

7 School of Life and Environmental Sciences, Deakin University, PO Box 423, Warrnambool, Victoria 3280, Australia

8 Centre for Ocean Studies, The University of Western Australia, 35 Stirling Highway, Crawley, Perth, Western Australia 6009, Australia

9 Fenner School of Environment and Society, Australian National University, Canberra, Australian Capital Territory 0200, Australia

10 Laboratoire des Substances Naturelles, Equipe d'Océanographie Biologique, Département de Biologie, Faculté des Sciences, BP.403, Agadir principale, 80.000, Agadir, Morocco

11 Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (ICM-CSIC), Passeig Maritím de la Barceloneta 37-49, 08003, Barcelona, Spain

12 Environmental and Marine Response, Biosecurity Response | Post-Border, MAF Biosecurity New Zealand, Ministry of Agriculture and Forestry, Te Manatu Ahuwhenua, Ngaherehere, New Zealand

13 National Institute of Water and Atmospheric Research (NIWA), PO Box 893, Nelson 7040, New Zealand

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BMC Evolutionary Biology 2011, 11:176  doi:10.1186/1471-2148-11-176

Published: 21 June 2011

Abstract

Background

Ecosystem 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.

Results

Extensive 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.

Conclusions

This 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.