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Phylogeny and Evolution of Marine Mussels

Introduction

The phylum Mollusca is the second largest phylum of animals, with about 130 000 named extant species and 70 000 described fossil species (Haszprunar et al. 2008). While most of these are marine, many live in freshwater and terrestrial habitats. Research has indicated that molluscs had a terminal Precambrian origin, with rapid divergence occurring in the Cambrian era some 540-560 million years ago (Stöger et al. 2013). All molluscs have a soft body that, with the exception of some groups (see later), is protected by a hard calcium shell. Inside the shell is a heavy fold of tissue called the mantle that encloses the internal organs of the animal. Another feature of the phylum is a large muscular foot that is generally used for locomotion. Although most molluscs share this basic body plan, the group is characterised by a great diversity of form and habit.

Phylogeny of the Phylum Mollusca

Eight living classes (lineages) of molluscs have been recognised, primarily based on clad1 (phylogenetic) analysis of morphological characters (Haszprunar et al. 2008). Aplacopora incorporates two classes, Solenogastres and Caudofoveata; these are worm-shaped, deep-water animals lacking a shell. Polyplacophora, often referred to as chitons, inhabit hard substrates on rocky shores and are characterised by eight dorsal shell plates. Aplacophora and Polyplacophora are grouped in the clade2 Aculifera, which is regarded as monophyletic (i.e. all taxa in this group share a common ancestor) (Sigwart & Sutton 2007). The remaining five classes are grouped in the clade Conchifera, which is also regarded as a monophyletic group. Monoplacophora live in deep waters and are small and limpet-like, with a single cap-like shell. The class Bivalvia includes laterally compressed animals enclosed in two shell valves, such as clams mussels, oysters and scallops. Scaphopoda, commonly known as tusk shells, live in marine mud and sediments. The class Gastropoda is the largest and most diverse, containing spirally coiled snails, flat-shelled limpets, shell-less sea slugs and terrestrial snails and slugs. Octopus, squid and cuttlefish are in the class Cephalopoda and represent the largest, most organised and specialised of all the molluscs. The Monoplacophora are generally accepted as the earliest extant offshoot of the Conchifera (Haszprunar 2008).

Morphological disparity among the lineages has given rise to numerous conflicting phylogenetic hypotheses. Molecular investigations using nuclear ribosomal gene sequences (18S and 28S) offered little resolution (Ponder & Lindberg 2008). More recent studies, using phylogenomic-scale molecular data sets (Kocot et al. 2011; Smith et al. 2011; Stöger et al. 2013), have significantly advanced understanding of molluscan phylogeny by providing well-supported tree topologies and generally congruent results (Telford & Budd 2011; Kocot 2013; Schrödl & Stöger 2014). Probably the most important achievement of these studies is the establishment of the Aculifera and Conchifera groupings.

Several major evolutionary hypotheses and sister relationships have been proposed for the eight living molluscan classes, which are illustrated in Figure 1.1 (Sigwart & Lindberg 2015). Sigwart & Lindberg (2015) assembled a data set of 42 unique published trees describing molluscan interrelationships, which included at least five out of the eight classes. They found that almost 60% of trees based on morphological data (N = 27) were similar, while only 45% of those based on molecular data (N = 15) were similar; the distances separating morphological and molecular trees indicated that they were similar in almost 30% of pairs and different in 20%. It is interesting that there are no studies in which both molecular and morphological data have been simultaneously analysed for all eight classes of Mollusca (Sigwart & Lindberg 2015). Regarding some of the hypotheses illustrated in Figure 1.1, the authors found that support for Cyrtostoma or Diasoma was relatively weak, while the Serialia concept was deserving of due consideration (see also Stöger et al. 2013). They found no consensus support for the topology of the morphological Testaria concept. Integration of new molecular techniques with morphological and developmental data using multiple type species from all eight molluscan classes will no doubt continue to deepen our understanding of molluscan phylogeny and evolution (Kocot 2013; Sigwart & Lindberg 2015).

Figure 1.1 Schematic topology of the major evolutionary hypotheses and sister relationships proposed for the eight living classes in Mollusca: Aculifera (Solenogastres + Caudofoveata + Polyplacophora), Aplacophora (Caudofoveata + Solenogastres), Conchifera (Monoplacophora + Bivalvia + Scaphopoda + Gastropoda + Cephalopoda), Cyrtosoma (Gastropoda + Cephalopoda; historically also including Monoplacophora), Diasoma (Bivalvia + Scaphopoda), Serialia (Polyplacophora + Monoplacophora), and Testaria (Conchifera + Polyplacophora). Text in bold indicate the seven different hypotheses.

Source: From Sigwart & Lindberg (2015). Reproduced with permission from Oxford University Press.

Phylogeny and Evolution of Bivalvia

Bivalvia is the second largest class within the Mollusca, with more than 9000 extant species. Individuals are bilaterally symmetrical with a laterally compressed body enclosed in two shell valves. Bivalves are an important component of marine and freshwater ecosystems, with more than 80% of species living in oceanic habitats and exhibiting varied ecologies. Sessile epifaunal bivalves, such as oysters and mussels, attach themselves to hard surfaces, while infaunal bivalves, such as clams, burrow to different depths in sand or sediment on the seafloor or in riverbeds. Other sessile forms bore into hard sediments such as coral and wood. Some species, such as scallops, are free-living and can move through the water by clapping the two shell valves together or dig into the sediment using their muscular foot. Although some bivalves are deposit feeders, the majority feed using greatly enlarged gill surfaces to filter food particles from the surrounding water. However, because of their mode of feeding, they pump large volumes of water and thus have the potential to accumulate contaminants, bacteria, viruses and toxins, frequently posing significant public health risks. Despite this, many species form the basis of valuable aquaculture and fisheries industries worldwide.

Although bivalves, with their strong shells, provide one of the most complete fossil record, their systematics3 until recently lagged behind that of other animal groups. Historically, there was a heavy reliance on single-character systems (e.g. shell hinge teeth, shell ligament, gill structure, gill ciliation and stomach morphology). This changed in the 1970s with the development of numerical systematics based on simultaneous analysis of multiple character systems. From the early 1990s, gene sequence data became available, and over the past two decades researchers have been increasingly involved in large-scale phylogenetic analyses using shell morphology and anatomy, fossils and, more recently, molecular sequence data. These data sources have made a significant contribution in systematic studies, encompassing all Bivalvia as well as major groups within the class (Carter et al. 2000; Harper et al. 2000; Giribet & Wheeler 2002 and references therein; Matsumoto 2003; Plazzi & Passamonti 2010; Plazzi et al. 2011; Tsubaki et al. 2011; Sharma et al. 2012; Yuan et al. 2012). Recently, Bieler et al. (2014) provided a new analysis of bivalve relationships integrating classic and novel morphological characters with a combination of up to nine molecular markers. While their results are largely consistent with many of the previous schemes of bivalve phylogenetics, they made significant progress in resolving previously uncertain relationships, which allowed them to refine higher order bivalve classification (Figure 1.2). Bieler et al. (2014) confirmed that the Bivalvia consists of two major clades, Protobranchia and Autobranchia (not shown in Figure 1.2), with the latter dividing into Pteriomorphia and Heterodonta (Heteroconchia). Heterodonta in turn consists of Archiheterodonta, Palaeoheterodonta and Euheterodonta. Protobranchia has been confirmed as a monophyletic group comprising Nuclida, Solemyida and Nuculanida - much in agreement with earlier morphology-based classifications. Protobranchs are primitive, marine, infaunal bivalves that use their large labial palps in deposit feeding - the ctenidia being used solely for respiration, in contrast to other subclasses within Bivalvia. They possess a lecithotrophic larval type, found in other primitive mollusc groups, as well as the respiratory pigment haemocyanin, found in nonbivalve groups such as cephalopods, polyplacophorans and gastropods (reviewed in Zardus 2002). Autobranchia, confirmed as the monophyletic sister group of Protobranchia, contains all of the remaining bivalve lineages. It is characterised by the presence of enlarged ctenidia with a...