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Patterns and Processes in the Biogeography of the Limpet Nacella (Mollusca: Patellogastropoda) Across the Southern Ocean Claudio A

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Patterns and Processes in the Biogeography of the Limpet Nacella (Mollusca: Patellogastropoda) Across the Southern Ocean Claudio A Journal of Biogeography (J. Biogeogr.) (2017) 44, 861–874 ORIGINAL Following the Antarctic Circumpolar ARTICLE Current: patterns and processes in the biogeography of the limpet Nacella (Mollusca: Patellogastropoda) across the Southern Ocean Claudio A. Gonzalez-Wevar1,2*, Mathias Hune€ 2, Nicolas I. Segovia2, Tomoyuki Nakano3, Hamish G. Spencer4, Steven L. Chown5, Thomas Saucede6, Glenn Johnstone7,Andres Mansilla1 and Elie Poulin2 1Universidad de Magallanes, Bulnes 01890, ABSTRACT Punta Arenas, Chile, 2Instituto de Ecologıa y Aim We use an integrative biogeographical approach to further understand the Biodiversidad (IEB), Departamento de evolution of an important Southern Ocean marine benthic element, the limpet Ciencias Ecologicas, Universidad de Chile, Las Palmeras 3425, Nu~ noa,~ Santiago, Chile, 3Seto genus Nacella (Mollusca: Patellogastropoda). Marine Biological Laboratory, Field Science Location Southern Ocean. Education and Research Centre, Kyoto University, Wakayama 649-2211, Japan, Methods We used multi-locus time-calibrated phylogeny of Nacella at the 4Allan Wilson Centre, Department of Zoology, scale of the whole Southern Ocean to elucidate the underlying processes University of Otago, Dunedin 9054, New involved in the origin and diversification of the genus. Zealand, 5School of Biological Sciences, Results Divergence-time estimates suggest that soon after its origin during the Monash University, Melbourne, VIC 3800, mid-Miocene (c. 12.5 Ma), Nacella separated into two main lineages currently Australia, 6Biogeosciences, UMR CNRS 6282, distributed in (1) South America and (2) Antarctica and the sub-Antarctic Universite de Bourgogne, Dijon 21000, islands. We identified two pulses of diversification, during the late Miocene (8 France, 7Australian Antarctic Division, < Kingston TAS 7050, Australia to 5.5 Ma) and the Pleistocene ( 1 Ma). Main conclusions Major periods of climatic and oceanographical change strongly affected the biogeography of Nacella and demonstrate both the long- and short-term influence of the Antarctic Circumpolar Current across the Southern Ocean. Our analyses support the validity of all currently recognized Nacella species and reveal a new South-American lineage. This work constitutes the most detailed molecular-based study of an ecologically important, near- shore invertebrate Southern Ocean group and in so doing contributes to the improved understanding of the underlying patterns and processes in the origin and diversification of marine benthic fauna across this globally important region. *Correspondence: Claudio A. Gonzalez-Wevar, Facultad de Ciencias, Universidad de Keywords Magallanes Antarctic Circumpolar Current, biogeography, lineage-through-time plots, E-mails: [email protected]; Nacella [email protected]. long-distance dispersal, , Southern Ocean significantly enhanced our knowledge of the biogeography of INTRODUCTION the region (Page & Linse, 2002; Strugnell et al., 2008; The origin, evolution and biogeography of the Southern Gonzalez-Wevar et al., 2010; Dıaz et al., 2011; Terauds et al., Ocean biota have long been controversial. Substantial differ- 2012; Saucede et al., 2014). Consensus is now growing about ences of opinion on the relative roles of vicariance versus the combined significance of vicariance and dispersal in dispersal and the relationships among different areas have explaining observed distributional patterns (Patarnello et al., characterized the literature since the early 1900s (Clarke 1996; Crame, 1999; Linse et al., 2006; Strugnell et al., 2008; et al., 1992; Aronson et al., 2007; Waters, 2008). New Fraser et al., 2009; Gonzalez-Wevar et al., 2010, 2012; Nikula research, as a consequence of extensive sampling campaigns et al., 2010; Mortimer et al., 2011; Cumming et al., 2014; and modern molecular laboratory techniques, has Poulin et al., 2014). ª 2016 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 861 doi:10.1111/jbi.12908 C. A. Gonzalez-Wevar et al. Early works relying on oceanographical evidence suggested sub-Antarctic Nacella species and those from Antarctica and that the Antarctic fauna was highly endemic and clearly South America remains poor. There is still no certainty divided into sub-Antarctic, low Antarctica and Antarctic/high about the number of species that are widespread and those Antarctic areas (Ekman, 1953; Hedgpeth, 1969). Recent anal- that are more narrowly distributed. For instance, the kelp- yses based on faunal similarities, however, have argued that dwelling N. mytilina is recorded from the southern tip of large-scale biogeographical patterns differ depending on the South America, the Falkland/Malvinas Islands and Kerguelen taxonomic group (Griffiths et al., 2009; Downey et al., 2012; Island, more than 8000 km away (Powell, 1973). Based on Pierrat et al., 2013; Griffiths & Waller, 2016). Moreover, the previous molecular studies showing that geographically approaches that integrate data from fossil, climatic, oceano- distant species fall in different genetic lineages (Gonzalez- graphical and genetic sources are revealing just how these Wevar et al., 2010), it might be expected that more than one differences play out among different taxonomic groups, while species is involved here. Nevertheless, considering the wide also providing insights into substantial cryptic diversity and geographical distribution of macroalgae (Fraser et al., 2009; spatial structuring within many of the groups (Leese et al., Macaya & Zuccarello, 2010), and many of their associated 2008; Strugnell et al., 2008; Gonzalez-Wevar et al., 2010, invertebrates (Helmuth et al., 1994; Waters, 2008; Nikula 2016; Arango et al., 2011; Baird et al., 2011; Dıaz et al., et al., 2010, 2012; Cumming et al., 2014), it is possible that 2011; Allcock & Strugnell, 2012). N. mytilina has a broad range across the sub-Antarctic. Simi- Comprehensive molecular studies of marine the fauna lar issues apply to N. macquariensis and N. kerguelenensis across the Southern Ocean nonetheless remain rare (e.g. recorded on the Kerguelen Plateau and at Macquarie Island, Thornhill et al., 2008; Fraser et al., 2009; Gonzalez-Wevar some 5000 km apart. et al., 2010; Dıaz et al., 2011). Indeed, most studies have In this study, we applied multi-locus molecular phyloge- been restricted to limited areas of the Southern Ocean netic reconstructions, divergence-time estimations including (Mahon et al., 2008; Wilson et al., 2009; Hunter & Hala- all the species currently found around the Southern Ocean. nych, 2010; Leese et al., 2010; Janosik et al., 2011). Hence, We derive a clear picture of the evolutionary relationships in much scope exists for multidisciplinary approaches using Nacella, the taxonomic status of different populations within broadly distributed taxa to improve understanding of the species and biogeography of the entire genus. We also com- biogeography and evolutionary history of this important pared the distribution of the evolutionary lineages in Nacella region (Chown et al., 2015). with the large-scale faunal provinces proposed for Southern The patellogastropod limpet genus, Nacella Schumacher, Ocean gastropods (Griffiths et al., 2009; Pierrat et al., 2013; 1817, occurs on many of the intertidal and subtidal shores Koubbi et al., 2014). Addressing these specific issues in the around the Southern Ocean and includes several species context of this dominant benthic group provides fresh endemic to one or two geographically isolated sub-Antarctic insights of the biogeography and evolution of the Southern islands (Powell, 1973). South America, and in particular the Ocean marine biota. Magellanic Province, shows the highest taxonomic richness, with at least eight nominal species (Powell, 1973; Valdovinos MATERIALS AND METHODS &Ruth,€ 2005). As a consequence, Powell (1973) argued that this region was the centre of origin for the genus, from Sample collection which seaweed-associated species spread eastward, driven by the West Wind Drift. Nevertheless, the role of long-distance Nacella species were collected from across the Southern dispersal in the evolution of the Southern Ocean’s biota has Ocean (see Appendix S1 in Supporting Information) and been controversial (Waters, 2008). Even Powell (1955) was identified following Powell (1973), Valdovinos & Ruth€ critical of this hypothesis and wrote: ‘too much stress ... laid (2005) and Gonzalez-Wevar et al. (2010, 2011; Fig. 1). Indi- on the apparent circum-sub-Antarctic range of molluscs that viduals from Heard Island identified as N. macquariensis are presumed to owe their distribution to the West Wind (Gonzalez-Wevar et al., 2010) are here referred as N. cf. mac- Drift’. As for many Southern Ocean molluscan (and other) quariensis (Appendix S1). Two specimens from Kerguelen groups that show conservative morphologies, including Island were sampled from living kelps, and based on shell Yoldia (Gonzalez-Wevar et al., 2012; Poulin et al., 2014), morphology (Powell, 1973), they are labelled as N. aff. myti- Trophon/Trophonella (Barco et al., 2012), Doris (Wilson lina Appendix S1 in Supporting Information. Finally, speci- et al., 2009) and Margarella (Williams et al., 2010; Williams, mens (n = 3) of a putative new species recently recorded at 2012), molecular studies have improved the understanding the Beagle Channel, southern South America, were also of the evolution of Nacella (Gonzalez-Wevar et al., 2010, included in the analysis. 2011; De Aranzamendi et al., 2011). Geographically distant species of Nacella generally exhibit greater genetic differentia-
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