Marine Mussels. Elizabeth Gosling
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 filtering function and comprises two sister taxa, the Pteriomorphia and Heteroconchia. The former is monophyletic and contains four well‐supported marine clades: Arcida (arks), Mytilida (mussels), Ostreida (oysters) and Pectinida + Limida (scallops) (Figure 1.2). A molecular analysis based on 42 mitochondrial genomes of phylogenetic relationships within the Pteriomorphia supports the monophyly of the Pteriomorphia (Sun & Gao 2017), although it includes an additional clade, Pterida, now accepted as Ostreida (http://www.marine species.org). Heterodonta is also confirmed as monophyletic and, as mentioned earlier, is composed of three clades, Palaeoheteterodonta, Archiheterodonta and Euheterodonta. Molecular analyses support a divergence of Archiheterodonta prior to the split of the other two clades, which have traditionally been grouped in the Heteroconchia but are now regarded as sister taxa (Bieler et al. 2014). The well‐supported Palaeoheteterodonta consists of the marine Trigoniida, remnants of a once diverse group, and the diverse freshwater Unionida (freshwater mussels, pearl mussels). The likewise well‐supported clade Archiheterodonta is monophyletic and comprises marine clams Carditida (González & Giribet 2014). Euheterodonta consists of two well‐supported clades, Anomalodesmata, a deep‐sea group of marine clams with unusual morphology, and the remaining Heterodonta, to which Bieler et al. (2014) have applied the name ‘Imparidentia’, a sister group to Anomalodesmata. The new clade Imparidentia, the relationships of which are not fully resolved (Bieler et al. 2014; González et al. 2015), includes some of the best‐known bivalves and most of the commercial species, excluding mussels, oysters and scallops, all of which are members of the Pteriomorphia.
Figure 1.2 Phylogenetic diagram showing hypothesised relationships between the major clades recognised for the living members of the class Bivalvia. While formal endings imply certain ranks in the Linnaean hierarchy, no attempt was made to re‐rank all hypothesised clades from Bieler et al.’s study (2014) as they considered ‘such a step as premature until a denser family‐level sampling is presented’.
Source: Based on Bieler et al. (2014).
Evolution and Adaptive Radiation in Bivalvia
As already mentioned, bivalves, because of their strong shells, provide one of the most complete fossil records of any animal group. The earliest known bivalves are the Early Cambrian (540 mya) Pojetaia runnegari from Australia, the Middle Cambrian (510 mya) Tuarangia gravgaerdensis from New Zealand and the Upper Cambrian (485 mya) Fordilla troyensis (details in Giribet 2008). These were all <1 cm in length and possessed a bivalved shell, a simple ligament, bivalve‐like pedal muscle insertions and well‐developed adductor muscle insertions (Morton 1992). According to Morton (1996), they were probably surface dwellers that used the foot for feeding and locomotion. Protobranchs closely resembling modern‐day representatives (Figure 1.2) were widespread by the early Ordovician (485 mya), as were all extant lineages and feeding types from most other lineages (see later). Protobranchs are clearly separated from the rest of the Bivalvia by a number of distinct morphological traits that are unique to the group (see earlier), but whether these represent an ancestral or a derived condition (i.e. traits that have evolved as a result of the clade's evolution) is not clear (Cope 2000 and references therein). Results from a comprehensive cladistic analysis that incorporated both morphological and molecular characters show that Protobranchia are basal to the entire Bivalvia class (Giribet & Wheeler 2002).
One of the