Phylogeny and systematics of Protodrilidae (Annelida) inferred with total evidence analyses

Abstract

Protodrilidae is a group of small, superficially simple-looking annelids, lacking chaetae and appendages, except for two prostomial palps. Originally considered to be one of the primitive "archiannelid" families, its affinity within Annelida is still highly debated. Protodrilids are found worldwide in the interstices of intertidal and subtidal marine sediments. Despite their simple appearance they constitute one of the most species-rich interstitial families, with 36 described species in two genera, Protodrilus and the gutless Astomus. Here we present the first phylogenetic study of Protodrilidae employing five gene fragments, 55 morphological characters and 73 terminals (including seven outgroups) analysed under direct optimization and parsimony as well as model-based methods. The large data set includes all 36 described species of Protodrilidae (17 of which are represented only by the morphological partition) as well as 30 undescribed or uncertain species (represented by both morphology and molecules). This comprehensive, inclusive and combined analysis revealed a new perspective on the phylogeny of Protodrilidae: the family is shown to contain six cosmopolitan subclades, each supported by several morphological apomorphies, and with the genus Astomus consistently nested among the other five clades rather than next to these. Consequently, the diagnosis of Protodrilus is emended, Astomus remains unchanged and the four remaining lineages are diagnosed and named Megadrilus n. gen, Meiodrilus gen. nov., Claudrilus n. gen and Lindrilus gen. nov. Character transformations showed that large size and presence of pigmentation, oviducts and eyes are plesiomorphies of the family, retained in Protodrilus, Megadrilus gen. nov. and Lindrilus gen. nov. These features are secondarily lost in the gutless Astomus with epidermal uptake of nutrients, as well as in Meiodrilus gen. nov. and some species of Claudrilus n. gen, with smaller size correlated to life in interstices of finer sediments.

The Evolution of Annelids Reveals Two Adaptive Routes to the Interstitial Realm

“…Polygordiidae, Saccocirridae, and certain species of Protodrilidae are several centimeters long and usually comprise numerous segments [9,29]. Instead, we propose that miniaturization explains evolution of these taxa ( Figure 3B), thereby contradicting the previous hypothesis of progenesis [4].…”

Trilobodrilus itoi sp. nov., with a Re-Description of T. nipponicus (Annelida: Dinophilidae) and a Molecular Phylogeny of the Genus

“…The effectiveness of incorporating DNA data in studies of meiofaunal taxonomy has become apparent for many taxa, including Nemertodermatida (Meyer-Wachsmuth et al, 2014), Proseriata (Casu and Curini-Galletti, 2006;Scarpa et al, 2015), Gastrotricha (Kieneke et al, 2012), Nemertea (Tulchinsky et al, 2012;Leasi and Norenburg, 2014), Annelida (Di Domenico et al, 2014c;Martínez et al, 2014), and Rotifera (Fontaneto, 2014). While our SEM observations revealed some subtle differences in ciliation pattern between T. itoi and T. nipponicus, before comparing their DNA sequences we were uncertain whether these two represented different species.…”

“…The family as currently diagnosed (Westheide, 1984) contains 16 species in three genera (Read, 2014). Dinophilids and other interstitial annelid families, such as Diurodrilidae (Worsaae and Rouse, 2008;Golombek et al, 2013), Nerillidae , Protodrilidae (Bailey-Brock et al, 2010;Di Domenico et al, 2013;Martínez et al, 2013Martínez et al, , 2014, and Saccocirridae (Di Domenico et al, 2014a, b, c) are important for understanding annelid evolution overall (Worsaae and Kristensen, 2005;Struck, 2006;Westheide, 2008) and the biogeography (Curini-Galletti et al, 2012) and macroevolutionary patterns (Rundell and Leander, 2010) of microscopic animals.…”

Two new meiofaunal species of Trilobodrilus (Dinophilidae, Annelida) from California, USA

“…Specific primer details, including references, are listed in Table 2. All PCR specifications, including visualization, purification, and sequencing follow that of Martínez et al (2015) and Gonzalez et al (2017).…”