Across Annelida, accessing the water column drives morphological and lifestyle modifications-yet in the primarily "benthic" scale worms, the ecological significance of swimming has largely been ignored. We investigated genetic,...
moreAcross Annelida, accessing the water column drives morphological and lifestyle modifications-yet in the primarily "benthic" scale worms, the ecological significance of swimming has largely been ignored. We investigated genetic, morphological and behavioural adaptations associated with swimming across Polynoidae, using mitogenomics and comparative methods. Mitochondrial genomes from cave and pelagic polynoids were highly similar, with non-significant rearrangements only present in cave Gesiella. Gene orders of the new mitogenomes were highly similar to shallow water species, suggestive of an underlying polynoid ground pattern. Being the first phylogenetic analyses to include the holopelagic Drieschia, we recovered this species nested among shallow water terminals, suggesting a shallow water ancestry. Based on these results, our phylogenetic reconstructions showed that swimming evolved independently three times in Polynoidae, involving convergent adaptations in morphology and motility patterns across the deep sea (Branchipolynoe), midwater (Drieschia) and anchialine caves (Pelagomacellicephala and Gesiella). Phylogenetic generalized least-squares (PGLS) analyses showed that holopelagic and anchialine cave species exhibit hypertrophy of the dorsal cirri, yet, these morphological modifications are achieved along different evolutionary pathways, i.e., elongation of the cirrophore versus style. Together, these findings suggest that a water column lifestyle elicits similar morphological adaptations, favouring bodies designed for drifting and sensing. Pelagic annelids are largely understudied, with poorly known origins, an unrecognized diversity and delicate bodies. Their mystery lies in their original discovery, which in most cases, dates back several centuries and are based on single observations of often incomplete or damaged specimens 1 . Yet, annelids are not uncommon throughout the oceanic water column, the midwater, with several groups containing only holopelagic species, including Lopadorrhynchidae, Iospilidae, Typhloscolecidae, Tomopteridae 2 , Alciopini, and Ctenophoricola 3 . Among the obligate holopelagic groups, evolution has driven numerous morphological specializations, including well-developed eyes (Alciopini), transparent bodies (Tomopteridae), specialized feeding and reproductive modes (Lopadorrhynchidae, Ctenophoricola) and creative defensive strategies (Alciopini 4,5 ; Swima 6 ). Holopelagic species are found within several other annelid families too, and are assumed to have evolved by opportunistic colonization events within otherwise benthic lineages. Such examples include Poeobius and Flota, two unrelated holopelagic genera within the otherwise benthic Flabelligeridae 7 , Swima and Teuthidodrilus within Acrocirridae 8 , Alciopini and Ctenophoricola within Phyllodocidae 3 and Chaetopterus pugaporcinus Osborn, Rouse, Goffredi & Robison, 2007 within the tube dwelling Chaetopteridae 9 . Several other annelid representatives can be found in the water column, but distinguishing truly pelagic forms from late stage larvae, or species with periodic swimming has proven challenging given the limited amount of direct observations available. Countless records of "benthic" annelids being collected from the water column are known 2 , but much work remains before we understand the true significance of benthic-pelagic interactions in annelids. Holopelagic species described from otherwise benthic groups often exhibit morphological adaptations that are convergent with those seen in exclusively holopelagic clades 2 . Regardless of their origin, annelids using the water column as habitat have undergone shifts in their behaviour and posture, specifically with regards to motility and lifestyle 10 . Some holopelagic species appear to swim continuously (e.g., Alciopini), many alternating between active swimming and drifting (e.g., Tomopteridae, Swima, Poeobius, and Flota) and others only drifting as in Chaetopterus pugaporcinus.