Incongruence between molecular phylogeny and morphological classification in amphipod crustaceans: A case study of Antarctic lysianassoids

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Abstract

In Antarctic waters, the superfamily Lysianassoidea is one of the most important amphipod groups both in terms of species number and abundance. Dominant members of this superfamily are species of the orchomenid complex, found throughout the Southern Ocean. This study presents the first molecular phylogenetic analysis based on a representative subset of the Antarctic species belonging to different orchomenid genera and hence provides a framework for a systematic revision of these taxa. The current classification of the orchomenid genera is mainly based on mouthpart morphology. The validity of these morphological characters was assessed by resolving phylogenetic relationships using nuclear 28S rRNA and mitochondrial cytochrome oxidase subunit I sequences. The molecular data rejected most of the previously proposed taxonomic subdivisions within this complex. The genera Abyssorchomene and Orchomenella as well as the subgenus Orchomenopsis appeared to be non-monophyletic. This implies that the supposed diagnostic characters are likely a result of convergent evolution. Further, our results indicated the necessity of a revision of the family-level systematics.

Introduction

For a long time, the concept of a global-scale increase in species richness from the poles to the equator (Clarke and Johnston, 2003) let assume that the Southern Ocean was depressed in species richness. Recently, the number of studies on Antarctic biodiversity and biogeography increased and challenged this view for several higher taxa. These studies suggested, in contrast, that the species richness in certain animal groups in the Southern Ocean might be comparable to this from temperate and tropical continental slopes in the Southern Hemisphere (Brandt et al., 2007), with species endemism rates of around 50% (Griffiths et al., 2009).

With more than 1500 strictly Antarctic species, the Southern Ocean is nowadays considered as a hotspot of biodiversity and that of endemisms for several orders of peracarid crustaceans (Malacostraca) like isopods and amphipods. Moreover, peracarids have undergone spectacular adaptive radiations in the Southern Ocean (Watling and Thurston, 1989, Brandt, 1999, Lörz and Brandt, 2004, Lörz and Held, 2004, Brandt, 2005). Among them, amphipods are the most diverse with more than 815 gammaridean and corophiidean species in the Southern Ocean sensu lato and more than 500 species from the Antarctic region only (De Broyer et al., 1999, De Broyer et al., 2003a, De Broyer et al., 2007).

The superfamily Lysianassoidea is one of the dominant gammaridean amphipod groups in Antarctic waters, both in number of species and abundance (Arnaud et al., 1986, De Broyer et al., 2001). Members of the group are common in deep oceanic basins as well as in shallow waters in high latitudes. Many species are scavengers and play a key role in deep-sea benthic communities by consuming and dispersing food falls of all sizes (Slattery and Oliver, 1986, De Broyer et al., 2004). In the Southern Ocean, dominant members of this superfamily are species of the orchomenid genus complex comprising the genera Abyssorchomene De Broyer, 1984, Falklandia De Broyer, 1985, Orchomenella G.O. Sars, 1895 (including the subgenera Orchomenella and Orchomenopsis), Orchomenyx De Broyer, 1984 and Pseudorchomene Schellenberg, 1926. The genera Falklandia, Orchomenyx and Pseudorchomene are endemic to the Southern Ocean sensu lato. Although the other two genera, Orchomenella and Abyssorchomene, may be considered as cosmopolitan (Barnard and Karaman, 1991), they also harbour some species endemic to the Southern Ocean.

Amphipods have a history of taxonomic instability concerning higher ranks: there has been much contention concerning their classification and phylogenetic relationships (Bousfield and Shih, 1994). In fact, higher-level relationships within Amphipoda are still so uncertain that several taxonomic treatments simply list families alphabetically (Barnard and Karaman, 1975, Barnard and Barnard, 1983, Barnard and Ingram, 1990, Martin and Davis, 2001). The masking effects of convergent or homoplastic morphology was reasserted as a major issue in amphipod taxonomy (Englisch et al., 2003, Macdonald et al., 2005, Hou et al., 2007, Fišer et al., 2008, Ito et al., 2008).

Despite several studies intending to clarify the systematics of the orchomenid genus complex (Shulenberger and Barnard, 1976, De Broyer, 1983, De Broyer, 1984, De Broyer, 1985a, Barnard and Karaman, 1991), the relationships among these taxa remain obscure (Table 1). The taxonomic history of this orchomenid genus complex dates back to Barnard (1964) who put the genera Orchomenella, Orchomenopsis and Allogaussia Schellenberg, 1926, in synonymy with Orchomene. In his revision of this group, De Broyer, 1983, De Broyer, 1984, De Broyer, 1985a, De Broyer, 1985b deemed that the morphology of mouthparts was of prime importance in the systematics of the Lysianassoidea. Taking this new set of morphological characters into account, he was able to identify a combination of characters that supported the revalidation of the genus Orchomenella, to combine Orchomenopsis to Orchomenella as a subgenus, together with Orchomenyx as a new subgenus, and to identify Abyssorchomene and Falklandia as new genera. Barnard and Karaman (1991) found these new generic characters very difficult to evaluate and considered, as a conservative measure, all these taxa but Pseudorchomene as a monophyletic assemblage within a supergenus Orchomene in the family Lysianassidae. Lowry and Stoddart (1997) raised Orchomenyx to the generic level and moved it together with Orchomenella and Pseudorchomene to the Tryphosinae. This subfamily was established within Lysianassidae, with the notable exception of Abyssorchomene and Falklandia which were omitted from that revision. The most recent systematic classification (De Broyer et al., 2007) followed Lowry and Stoddart (1997) and corrected those omissions in placing Falklandia in the Lysianassidae (Tryphosinae), and Abyssorchomene within the Uristidae.

Given this framework, the present study aims at resolving the phylogenetic relationships of the orchomenid complex of genera of the Southern Ocean and testing the validity of the morphological characters used for their taxonomy. This study is the first molecular phylogenetic analysis of a representative subset of this species assemblage, using DNA sequences of the mitochondrial cytochrome oxidase subunit I (COI) and the nuclear 28S rRNA genes. It could serve as a basis for further systematic studies of this dominant group in the Southern Ocean.

Section snippets

Sampling

Specimens were collected with the research vessel Polarstern during several Antarctic expeditions: EASIZ II (ANTARKTIS XV-3, De Broyer et al., 1999), LAMPOS (ANTARKTIS XIX-5, De Broyer et al., 2003b), ANDEEP I, II, III (De Broyer et al., 2003b, De Broyer et al., 2006), ANTARKTIS XXIII-8 (d’Udekem d’Acoz and Robert, 2008). These campaigns provided shelf and deep-sea samples from the Scotia Sea, the Scotia Arc, the eastern shelf of the Antarctic Peninsula, the Weddell Abyssal Plain, the eastern

Results

In total, COI and 28S sequences of 46 specimens were obtained (see Table 2). The aligned COI sequences consisted of 658 positions. No stop codons were observed and DNA sequences showed higher mutation rates in third codon positions which is typical for protein-coding genes. The matrix of aligned 28S sequences contained 1334 positions. The combined dataset was 1992 base pairs in length, 534 positions were parsimony informative (140 bp of COI and 394 of 28S).

According to our preliminary molecular

Polyphyly of some orchomenid genera

Phylogenetic patterns revealed by our molecular study consistently differ from the traditional, morphology-based taxonomy in many respects, and casts doubt on the monophyly of some of the genera currently used in the lysianassoid systematics. Two orchomenid genera are clearly polyphyletic. The most striking example is Abyssorchomene. This genus is found in three clades and it may be paraphyletic or monophyletic in each of them. The genus Orchomenella is polyphyletic, as its subgenus

Acknowledgments

The first author is financially supported by an “Action II” grant (contract number WI/36/H04) from the Belgian Science Policy Office (Belspo). Sampling in Antarctic regions was supported by the Scientific Research Programme on the Antarctic of Belspo (contract numbers A4/DD/B02 and EV/36/24A). For genetic analyses, funding was provided by the Joint Experimental Molecular Unit (project BARCOLYS) that is supported by Belspo. We thank the crew of the R/V Polarstern for their professional

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