Cryptic species and colonization processes in Ophryotrocha (Annelida, Dorvilleidae) inhabiting vertebrate remains in the shallow‐water Mediterranean

Abstract

Over the past several years, there has been growing interest in how bones of decaying mammals are colonized in the marine seabed. One of the most common opportunistic taxa occurring worldwide on bones is dorvilleid polychaetes of the genus Ophryotrocha. In a recent study in the Mediterranean, Ophryotrocha puerilis and Ophryotrocha alborana were two of the most abundant species occurring in experimentally deployed bones. These species have direct development and this makes them a suitable model to study the mechanisms and processes allowing organisms lacking a dispersive larval phase to colonize new substrates. Here, we address the colonization processes at the molecular level for populations of O. puerilis and O. alborana on experimentally deployed mammal bones in the shallow‐water Mediterranean collected over a year at 3‐month intervals. High genetic distances between some of the O. puerilis organisms collected indicated the occurrence of at least two cryptic sibling species (O. puerilis ‘Shallow’ and O. puerilis ‘Deep’) apart from O. puerilis sensu stricto. This was corroborated with phylogenetic analyses using an alignment of three concatenated genes (COI, 16S, H3) and with species delimitation analyses using COI. The haplotype network inferred from COI sequences for O. puerilis ‘Shallow’ showed a few common haplotypes shared between the two trimesters analysed and several other less represented haplotypes only present in one trimester. Thus, colonization of these experimental bones may have been achieved by a few organisms that arrived to the bones and were able to reseed, and by several individuals arriving to the experimental bones and not persisting across time. In contrast, the haplotype network for O. alborana revealed that none of the haplotypes present in three different trimesters were shared, suggesting that the populations arriving at the bones during each trimester were totally replaced by new individuals during the subsequent trimesters. Our study suggests that different species of shallow‐water Ophryotrocha occurring in the Mediterranean may have different patterns of substrate colonization despite sharing similar life histories.

The Current State of Eunicida (Annelida) Systematics and Biodiversity

“…A detailed description of the external and internal morphology of Dorvilleidae is available in Wiklund et al [69]. Due to their small size and frequently minor morphological differences, dorvilleids can be difficult to identify correctly, and different species are often only detected following molecular analysis (e.g., [44]).…”

“…Nevertheless, apart from a few records of estuarine occurrence, dorvilleids seem to be predominantly fully marine organisms. Species of the genera Ophryotrocha and Parougia are particularly common and frequently highly abundant in organically enriched habitats, such as harbors, fish farms, sewage discharges and organic-falls (wood or the carcasses of large animals sunken to the seafloor) [16,31,44,[72][73][74][89][90][91][92], being considered by some authors as nonspecialized opportunists (e.g., [48]). These two genera, along with Exallopus, include the majority of the species occurring in deeper waters [19,67,[93][94][95][96][97], often in extreme habitats such as hydrothermal vents and cold seeps [18,[97][98][99][100][101][102].…”

“…The exploration of organically enriched areas led to a great increase in the number of Ophryotrocha and Parougia species (e.g., [16,18,31,44,[72][73][74]92,[96][97][98][99][100][101][102]110]). The occurrence of several sympatric congeners is also frequently reported for both genera (e.g., [16,18,31,44,[72][73][74][111][112][113]). Furthermore, with the upswing in deep-sea exploration, more species of these and other genera have been described also from areas that seemingly were not organically enriched (e.g., [19,93,94,[114][115][116]).…”

“…All families have records of widely distributed species, which deserve further investigation. Most widespread species studied in detail ended up as more than one species [43][44][45] or exotic species dispersed by human mediated transport [46,47]. However, some species appear to have naturally widespread distributions [48,49] despite the poor natural dispersal capability attributed to eunicidan species.…”

Polychaetes of Greece: an updated and annotated checklist

“…Simboura and Nicolaidou (2001) report Ophryotrocha puerilis from Greece at species level, as it is reported on other parts of the Mediterranean as well (Castelli et al 2008, Çınar et al 2014, Núñez et al 2013, Mikac 2015). However, Taboada et al (2017) provide molecular evidence of at least two cryptic species under the name Ophryotrocha puerilis in the Mediterranean Sea.…”