Concerted Genetic, Morphological and Ecological Diversification In
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Molecular Ecology (2011) 20, 1936–1951 doi: 10.1111/j.1365-294X.2011.05065.x Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province C. A. GONZA´ LEZ-WEVAR,* T. NAKANO,† J. I. CAN˜ ETE‡ and E. POULIN* *Instituto de Ecologı´a y Biodiversidad, Departamento de Ciencias Ecolo´gicas, Facultad de Ciencias, Universidad de Chile, Las Palmeras # 3425, N˜ un˜oa, Santiago, Chile, †Department of Geology and Paleontology, National Museum of Nature and Science, Tokyo, Japan, ‡Departamento de Recursos Naturales, Universidad de Magallanes, Punta Arenas, Chile Abstract Common inhabitants of Antarctic and Subantarctic rocky shores, the limpet genus Nacella, includes 15 nominal species distributed in different provinces of the Southern Ocean. The Magellanic Province represents the area with the highest diversity of the genus. Phylogenetic reconstructions showed an absence of reciprocal monophyly and high levels of genetic identity among nominal species in this Province and therefore imply a recent diversification in southern South America. Because most of these taxa coexist along their distribution range with clear differences in their habitat preferences, Nacella is a suitable model to explore diversification mechanisms in an area highly affected by recurrent Pleistocene continental ice cap advances and retreats. Here, we present genetic and morphological comparisons among sympatric Magellanic nominal species of Nacella. We amplified a fragment of the COI gene for 208 individuals belonging to seven sympatric nominal species and performed geometric morphometric analyses of their shells. We detected a complete congruence between genetic and morphological results, leading us to suggest four groups of Nacella among seven analysed nominal species. Congruently, each of these groups was related to different habitat preferences such as bathymetric range and substrate type. A plausible explanation for these results includes an ecologically based allopatric speciation process in Nacella. Major climatic changes during the Plio-Pleistocene glacial cycles may have enhanced differentiation processes. Finally, our results indicate that the systematics of the group requires a deep revision to re-evaluate the taxonomy of Nacella and to further understand the Pleistocene legacy of the glacial cycles in the southern tip of South America. Keywords: adaptive radiation, ecological speciation, Nacella, Patagonia, Patellogastropoda, Southern Ocean Received 5 November 2010; revision received 27 January 2011; accepted 9 February 2011 2004, 2007). Typically, taxonomic studies in the group Introduction have been based on shell morphology and external True limpets of the order Patellogastropoda are the characters, but the high degree of variability and homo- basal group in the evolution of Gastropoda, as revealed plasy detected in form and coloration has led to taxo- by morphological and molecular studies (Ponder & nomic confusion (Ridgway et al., 1998; Sasaki 1999; Lindberg 1997; Lindberg 1998; Harasewych & McArthur Espoz et al. 2004; Nakano & Spencer 2007; Lindberg 2000; McArthur & Harasewych 2003; Nakano & Ozawa 2008). Recent molecular studies have greatly improved the systematics and taxonomy of Patellogastropoda at the levels of family, genus and species. Seven families, Correspondence: C. A. Gonza´lez-Wevar, Fax: 056 02 2727363; Lotiidae, Acmaeidae, Pectinodontidae, Patellidae, E-mail: [email protected] Lepetidae, Eoacmaeidae and Nacellidae, are currently Ó 2011 Blackwell Publishing Ltd CONCERTED EVOLUTION IN MAGELLANIC LIMPETS 1937 recognized in the order using different molecular ward through the west wind drift. However, this markers (Nakano & Ozawa 2007). hypothesis has been rejected by recent phylogenetic Nacellidae includes two genera, Cellana and Nacella, analyses that showed that the Magellanic species of with clearly disjoint distributions (Powell 1973; Lind- Nacella are the most derived clade in the genus (Gonza´lez- berg 1998, 2008). Cellana has more than 37 species and Wevar et al. 2010a). Based on morphological studies, at subspecies mainly distributed in tropical to warm- least seven species of Nacella have been described for temperate waters of the Indo-Pacific regions (Powell the Magellan Province, but the taxonomy of the genus 1973; Lindberg 1998). Its distribution range includes in this region is still unclear (Table 1). Powell (1973) southern South Africa, the east coast of Africa, Egypt, recognized five valid taxonomic units: N. deaurata, the Arabian Sea and expands eastward as far north as N. flammea, N. fuegiensis, N. magellanica and N. mytilina, Japan. Recently, one species of Cellana was reported in one ecomorph (N. deaurata form delicatissima) and the Atlantic coast of Africa, but it appears to have been two subspecies (N. magellanica venosa and N. magella- introduced from Indo-Pacific regions (Nakano & Espin- nica chiloensis). Recently, Valdovinos & Ru¨ th (2005) in a osa 2010). Cellana is also distributed in oceanic islands revision of Nacella from southern South America con- of the Indian and Pacific Oceans such as the Bonin cluded that all the morphological species described in Islands, Guam, the Hawaiian islands, Society Island the Magellanic Province, with the exception of N. fuegi- and the Juan Fernandez archipelago in the East Pacific. ensis (considered as synonym of N. magellanica by the Finally, its southernmost distribution reaches Australia authors), are true taxonomic units with diagnostic dif- and New Zealand, as far south as subantarctic islands ferences in shell morphology (thickness and coloration), such as Auckland, Snares, Bounty, Antipodes, Chatham, mantle tentacles, foot coloration and radular tooth mor- and Campbell. In the Campbell islands, Cellana strigilis phology. strigilis co-exists with its sister genus Nacella, specifically The Magellanic species of Nacella also display ecologi- N. terroris (Powell 1973). The genus Nacella comprises cal, bathymetrical and latitudinal distribution differ- 15 nominal species mainly distributed in four of the ences (Morriconi & Calvo 1993; Morriconi 1999; Rı´os described biogeographical provinces of the Southern et al. 2003; Bazterrica et al. 2007). The species N. magel- Ocean (Griffiths et al. 2009): Antarctica, the Magellanic lanica, N. deaurata, N. delicatissima and N. fuegiensis are Province and subantarctic islands of the Antipodean commonly found in intertidal rocky environments, and Kerguelenian provinces (Powell 1973). One South while N. flammea and N. mytilina are subtidal (Fig. 1a). American species, Nacella clypeater, expands its distribu- Most of the species live attached to rocky substrates tion north up to Arica (Peruvian) along the Humboldt where they graze on microalgae, diatoms and bacterial Current System (Valdovinos & Ru¨ th 2005). films. Only N. mytilina lives exclusively attached to kelp In the Magellanic Province, Nacella represents one of such as Macrocystis pyrifera (Valdovinos & Ru¨ th 2005) the dominant groups of marine benthic macroinverte- and Lessonia flavicans (C.A. Gonza´lez-Wevar, personal brates, especially on rocky boulders and rocky shores observation). In terms of geographical distribution, all along the Magellan Strait and Patagonia (Guzma´n N. delicatissima, N. magellanica and N. deaurata have a 1978; Rı´os et al. 2003; Bazterrica et al. 2007). According wide distribution, from Chiloe´ Island in the Pacific to to Powell (1973), and considering that more than 50% the Buenos Aires in the Atlantic, including the Magellan of the species have been described from this Province, Strait, Tierra del Fuego, Southern Patagonia and the it has been considered as the centre of origin and diver- Falkland Islands (Powell 1973; Valdovinos & Ru¨th 2005). sification of the genus, from whence it expanded east- Other species such as N. flammea and N. fuegiensis exhibit Table 1 Taxonomy of Nacella in the Magellanic Province according to four different studies. Filled squares (grey) indicate how the particular study supports synonymies between and among taxa Nominal species Powell (1973) Valdovinos & Ru¨ th (2005) de Aranzamendi et al. (2009) This study N. fuegiensis N. fuegiensis N. magellanica n.i. N. deaurata N. deaurata N. deaurata N. deaurata N. deaurata N. delicatissima N. delicatissima Ecotype of N. magellanica or N. deaurata n.i. N. magellanica N. magellanica N. magellanica N. magellanica N. magellanica N. chiloensis N. chiloensis n.i. N. venosa N. venosa n.i. N. mytilina N. mytilina N. mytilina N. mytilina N. mytilina N. flammea N. flammea N. flammea n.i. N. flammea n.i., not included in the analyses. Ó 2011 Blackwell Publishing Ltd 1938 C. A. GONZA´ LEZ-WEVAR ET AL. (a) Nacella magellanica 2 m Nacella deaurata 1 m –1 m Nacella Nacella mytilina fuegiensis –5 m –10 m Nacella flammea –25 m (b) –80º –75º –70º –65º –60º –55º –80º –75º –70º –65º –60º –55º –80º –75º –70º –65º –60º –55º –30º –30º –30º –30º (i) (ii) (iii) –35º –35º –35º –35º –40º –40º –40º –40º –45º –45º –45º –45º –50º –50º –50º –50º –55º –55º –55º –55º –80º –75º –70º –65º –60º –55º –80º –75º –70º –65º –60º –55º –80º –75º –70º –65º –60º –55º Fig. 1 (a) Bathymetrical distributions of the nominal species of Nacella in Punta Santa Ana, Magellan Strait. (b) Latitudinal distribu- tion of the analysed nominal species of Nacella along the Magellan Province based on the descriptions of Powell (1973) and Valdovi- nos & Ru¨ th (2005). (i) N. magellanica, N. deaurata; (ii) N. flammea, N. fuegiensis and N. mytilina; (iii) N. chiloensis and N. venosa. a narrower distribution,