Progenetic dwarf males in the deep-sea wood-boring genus Xylophaga (Bivalvia: Pholadoidea)

Sunken plant debris (sunken wood, hereafter) in deep-sea environments harbours an idiosyncratic fauna that is based directly or indirectly on wood decomposition (Turner, 1973, 1978). This resource is ecologically comparable with deep-sea whale-falls, because of its ephemeral nature (Distel et al., 2000). The obligate wood-boring and wood-consuming (xylophagous) bivalve genera Xylophaga, Xylopholas and Xyloredo, all belonging to the family Xylophagaidae (Turner, 2002; we here regard it as an independent family based on unpublished molecular phylogenetic data of TH), occur primarily in the deep sea, extending down to the hadal zone, from polar to tropical regions (Knudsen, 1961; Schiotte, 2005). They have been recognized as the most important organisms that convert refractory sunken wood into a food source available to other members of the community (Turner, 1973; Distel & Roberts, 1997; Distel, 2003). However, Xylophagaidae remain little studied, as they are difficult to find due to their patchy distribution at great depths. Therefore, many species are known only from the type localities (see Voight, 2007). The reproduction of Xylophagaidae is poorly known so far. Purchon (1941) reported protandric hermaphroditism in Xylophaga dorsalis (Turton, 1819), but this interpretation was recently corrected by Tyler, Young & Dove (2007) to gonochoristic based on a reanalysis of Purchon’s (1941) data. Tyler et al. (2007) also showed gonochorism with a fast growth rate and rapid gametogenesis (in addition to very few examples of simultaneous hermaphroditism) in X. depalmai Turner, 2002. Purchon (1941) and Culliney & Turner (1976) suggested selffertilization for X. dorsalis and X. atlantica Richards, 1942, because both species have paired seminal vesicles (i.e. vesicles in which spermatozoa discharged from the same individual are stored) beneath the pedal retractor in the suprabranchial cavity. Such reproductive patterns have been regarded as a resource adaptation to their deep-sea ephemeral habitats (Purchon, 1941; Culliney & Turner, 1976; Tyler et al., 2007). On the other hand, extended parental care in the form of ‘juvenile brooding’ has often been suggested based on the occurrence of tiny individuals with pediveliger morphologies that are byssally attached to the shell or the soft parts of large Xylophaga individuals (Knudsen, 1961, 1967; Harvey, 1996; Turner, 2002; Voight, 2007, 2008, 2009). However, this proposed developmental mode remained puzzling, because the absence of pelagic larval development implies a low capacity for dispersal and for finding ephemeral resources in the deep sea (Knudsen, 1961; Scheltema, 1994; Voight, 2009). An alternative hypothesis concerning the association of tiny individuals with larger conspecifics in many Xylophaga species is that, instead of externally-brooded offspring, they represent mating partners in the form of dwarf males. Dwarf males are, in general, tiny individuals (50% or less of the normal body size) that attach to large individuals in gonochoristic organisms. They are believed to have evolved among species whose population size is small and/or in which the female is sedentary or hard to find (e.g. Ghiselin, 1974; Vollrath, 1998). The goal of our study was critically to test these two hypotheses by performing a detailed ultrastructural and histological study of tiny conspecifics attached to large individuals of X. supplicata (Taki & Habe, 1950). This species is found in the Western Pacific from Japan to the Philippines at depths of 200–5050 m (Higo, Callomon & Goto, 1999; Haga, 2011). Adults attain a maximum shell length (SL) . 15 mm. Xylophaga supplicata can colonize a wide range of submerged wooden substrates, ranging from tree trunks to bamboo branches and even individual mangrove seeds and it exhibits a low population density (T. Haga, unpubl.). Materials examined in this study included the holotype (National Museum of Nature and Science, Tokyo; Mo-39891) in addition to 54 large specimens that had bored into wooden substrates retrieved from waters around Leyte and Bohol, Philippines (n 1⁄4 38) and Espiritu Santo,Vanuatu (n 1⁄4 16). Live animals were carefully removed from the sunken wood by hand, anaesthetized, fixed in 10% seawater-diluted formalin, stored in 70% ethanol, then examined either by freeze-dried scanning electron microscopy (SEM) or by paraffin-embedded serial sectioning. The tiny conspecifics of X. supplicata attach byssally to the surface of the autonomously boring larger conspecifics, either singly or in multiples up to a maximum of 29. There are three areas of attachment: the periostracal extension on the dorsal and ventral side of the posterior slope, and the anterior umbonal area around the mesoplax (Fig. 1; circles). The holotype bears two tiny conspecifics (Fig. 1C); 45 out of the 54 autonomously boring individuals from the West Pacific (83.3%) carried tiny conspecifics. The number of the attached tiny conspecifics increased with host size (R 1⁄4 0.54, P, 0.001), suggesting that