Molecular systematics and global phylogeography of angel sharks (genus Squatina)

Abstract

Angel sharks of the genus Squatina represent a group comprising 22 extant benthic species inhabiting continental shelves and upper slopes. In the present study, a comprehensive phylogenetic reconstruction of 17 Squatina species based on two mitochondrial markers (COI and 16S rRNA) is provided. The phylogenetic reconstructions are used to test biogeographic patterns. In addition, a molecular clock analysis is conducted to estimate divergence times of the emerged clades. All analyses show Squatina to be monophyletic. Four geographic clades are recognized, of which the Europe–North Africa–Asia clade is probably a result of the Tethys Sea closure. A second sister group relationship emerged in the analyses, including S. californica (eastern North Pacific) and S. dumeril (western North Atlantic), probably related to the rise of the Panamanian isthmus. The molecular clock analysis show that both lineage divergences coincide with the estimated time of these two geological events.

Introduction

The angel shark genus Squatina (Chondrichthyes: Elasmobranchii: Neoselachii: Squalea: Squatinidae) comprises 22 extant, morphologically homogenous, benthic species (cf. Vooren and Da Silva, 1992, Compagno et al., 2005, Castro-Aguirre et al., 2006, Last and White, 2008), which inhabit continental shelves and upper slopes down to 500 m (Compagno et al., 2005). They are moderately-sized (total length about 1–2 m) and globally distributed in temperate to tropical seas (Compagno et al., 2005, Last and White, 2008). While some species occur over a wide geographic range, the majority are restricted to a smaller area (Compagno et al., 2005). Restriction in geographic range might be as a result of the behavior of Squatina species, which are ambush predators with a corresponding stationary bottom-dwelling habit (Compagno et al., 2005). Thus, trans-ocean migration is extremely unlikely, even though large-scale coastal migratory patterns have been reported in species such as S. squatina (Wheeler et al., 1975) and S. californica (Kato et al., 1967, Eschmeyer et al., 1983, Natanson and Cailliet, 1986, Compagno et al., 2005).

Based on their distribution, eight distinct putative zoogeographic species groups can be distinguished (distribution areas based on Compagno et al., 2005, Last and White, 2008): (1) Eastern North Atlantic–Mediterranean–North Africa (S. aculeata, sympatric with S. oculata and S. squatina in the Mediterranean), (2) southwest Indian Ocean, South Africa (S. africana), (3) western North Pacific, i.e. Asian species (S. formosa, S. japonica, S. nebulosa and S. tergocellatoides), (4) western South Pacific and eastern Indian Ocean, i.e. Australian species (S. australis along the south coast of Australia, partly sympatric with S. albipunctata along south-eastern Australia and with S. tergocellata along south-western Australia; S. pseudocellata occurs along north-western Australia) and S. legnota, which is recorded from Indonesia, (5) eastern North Pacific (S. californica), (6) eastern South Pacific (S. armata), (7) western North Atlantic (S. dumeril, sympatric with S. heteroptera and S. mexicana in the Gulf of Mexico) and (8) western South Atlantic (S. argentina, sympatric with S. guggenheim, S. occulta and S. punctata). These species groupings can be used to formulate and test biogeographic hypotheses, such as the influence of the rise of the Panamanian isthmus and the Tethys Sea closure on speciation.

Interspecific relationships of angel sharks have not been investigated except for a study by Furtado-Neto and Carr (2002) on three Brazilian species. The position of the squatinids within the elasmobranchs (sharks, skates and rays) based on morphological characters is still widely debated (cf. Compagno, 1973, Maisey, 1984, Thies and Reif, 1985, Seret, 1986, Shirai, 1992, de Carvalho, 1996). Recent mtDNA and nDNA studies by Douady et al. (2003) and Winchell et al. (2004) show closer relationships between Squatiniformes (angel sharks), Pristiophoriformes (saw sharks) and Squaliformes (dogfish sharks), which is congruent with morphological data.

In the present paper we present the first comprehensive phylogeography of the squatinid sharks based on two mitochondrial markers, cytochrome oxidase subunit I (COI) and 16S rRNA, using different tree reconstruction methods. In addition, fossil and geological calibration points are used to estimate divergence times among the Squatina species and to test biogeographic patterns of inferred species groups.