Cryptic speciation yields remarkable mimics: A new genus of sea slugs that masquerade as toxic algae (Caulerpa spp.)

Abstract

Abstract“Cryptic” can refer to species that match their background through camouflage or disruptive colouration, or in taxonomy to externally similar but unrecognized congeners. In adaptive resemblance, organisms resemble parts of a larger host animal or plant on which the mimic is highly cryptic. Mimetic lineages that radiate onto superficially similar hosts may contain cryptic species in both senses: taxa that are difficult to detect, and challenging for taxonomists to distinguish. Here, we describe a new genus and four species of herbivorous sea slugs (Gastropoda, Heterobranchia, Sacoglossa), including remarkable mimics of toxic green algae (Caulerpa spp.) on which the slugs feed. The long‐recognized Stiliger smaragdinus Baba 1949 is highly mimetic of “sea grapes” (Caulerpa racemosa‐lentillifera), but phylogenetic analyses of four genes indicated Stiliger was polyphyletic: the name‐bearing species grouped within Placida, whereas Caulerpa‐mimetic lineages were phylogenetically distinct. We erect the genus Sacoproteus gen. n. for S. smaragdinus (Baba 1949), and describe four new species: S. nishae sp. n. from the Indo‐Pacific, which mimics Caulerpa chemnitzia; Sacoproteus yhiae sp. n. and Sacoproteus browni sp. n. from southern Australia, which mimic Caulerpa cactoides and Caulerpa gemminata; and Sacoproteus thomasleei sp. n., a non‐mimetic west Pacific species that shared key features. Stiliger s.s. and Placida species show crypsis and aposematism but not host mimicry, although Stiliger spp. feeding on undefended algae may be Batesian mimics. Investigating the ecology and biogeography of Sacoproteus gen. n. will yield insight into how selection generates such extraordinary examples of adaptive resemblance in the marine realm.

Phylogenomic resolution of the root of Panpulmonata, a hyperdiverse radiation of gastropods: new insight into the evolution of air breathing

“…; 'Ercolania boodlea' is non-Ercolania Trinchese, 1872 [39], and 'Stiliger sp.' is of uncertain affinity given a polyphyletic Stiliger [40]. The only unsampled sacoglossan genera with ≥5 spp.…”

“…Briefly, specimens were collected under permits by the authors or colleagues and identified by morphology and placement in reference phylogenies. Undescribed species were provisionally numbered [39,40]. Specimens were maintained without food for several days to clear their digestive system, preserved in RNAlater and frozen at −80°C prior to extraction.…”

Natural history clues to the evolution of bivalved gastropods (Mollusca: Gastropoda: Sacoglossa: Juliidae)

“…The term latok in several regional languages refers to either of these two Caulerpa species as harvested for food. The broad feeding habits of B. singaporensis stand in contrast to other sacoglossan lineages that feed on Caulerpa and target a specific place on a specific species of food-plant, such as a preference for feeding by sucking on ramuli (Krug et al 2018). We speculate that B. singaporensis targets Caulerpa species based on the abiotic context of the microhabitat, perhaps driven by factors such as temperature or current flow; that is, while this microhabitat may correlate with the preferred habitat of particular Caulerpa spp., individual Berthelinia do not show clear preference among Caulerpa spp.…”

“…A large number of sacoglossan species remain undescribed, and ongoing work continues to reveal both new discoveries and cryptic species worldwide (e.g. Carmona et al 2011;Krug et al 2013;Espinoza et al 2014;Krug et al 2018). Jensen (1997) predicted that there might be a co-evolutionary or correlative relationship between sacoglossan diversity and the evolution of their food plants and that these relationships might have some predictive power about the number of species in genus-or family-level groups within Sacoglossa.…”

“…Investigations of other Sacoglossa in SE Asia have revealed pseudocryptic sibling species with apparently overlapping niches, sometimes co-occurring and even depending on the same food plant (e.g. Krug et al 2018).…”