Multigene phylogeny of the scyphozoan jellyfish family Pelagiidae reveals that the common U.S. Atlantic sea nettle comprises two distinct species (Chrysaora quinquecirrhaandC. chesapeakei)

Abstract

BackgroundSpecies of the scyphozoan family Pelagiidae (e.g.,Pelagia noctiluca,Chrysaora quinquecirrha) are well-known for impacting fisheries, aquaculture, and tourism, especially for the painful sting they can inflict on swimmers. However, historical taxonomic uncertainty at the genus (e.g., new genusMawia) and species levels hinders progress in studying their biology and evolutionary adaptations that make them nuisance species, as well as ability to understand and/or mitigate their ecological and economic impacts.MethodsWe collected nuclear (28SrDNA) and mitochondrial (cytochromecoxidase I and16SrDNA) sequence data from individuals of all four pelagiid genera, including 11 of 13 currently recognized species ofChrysaora. To examine species boundaries in the U.S. Atlantic sea nettleChrysaora quinquecirrha, specimens were included from its entire range along the U.S. Atlantic and Gulf of Mexico coasts, with representatives also examined morphologically (macromorphology and cnidome).ResultsPhylogenetic analyses show that the genusChrysaorais paraphyletic with respect to other pelagiid genera. In combined analyses,Mawia, sampled from the coast of Senegal, is most closely related toSanderia malayensis, andPelagiaforms a close relationship to a clade of PacificChrysaoraspecies (Chrysaora achlyos, Chrysaora colorata,Chrysaora fuscescens, andChrysaora melanaster).Chrysaora quinquecirrhais polyphyletic, with one clade from the U.S. coastal Atlantic and another in U.S. Atlantic estuaries and Gulf of Mexico. These genetic differences are reflected in morphology, e.g., tentacle and lappet number, oral arm length, and nematocyst dimensions. Caribbean sea nettles (Jamaica and Panama) are genetically similar to the U.S. Atlantic estuaries and Gulf of Mexico clade ofChrysaora quinquecirrha.DiscussionOur phylogenetic hypothesis for Pelagiidae contradicts current generic definitions, revealing major disagreements between DNA-based and morphology-based phylogenies. A paraphyleticChrysaoraraises systematic questions at the genus level for Pelagiidae; accepting the validity of the recently erected genusMawia, as well as past genera, will require the creation of additional pelagiid genera. Historical review of the species-delineating genetic and morphological differences indicates thatChrysaora quinquecirrhaDesor 1848 applies to the U.S. Coastal AtlanticChrysaoraspecies (U.S. Atlantic sea nettle), while the nameC. chesapeakeiPapenfuss 1936 applies to the U.S. Atlantic estuarine and Gulf of Mexico Chrysaora species (Atlantic bay nettle). We provide a detailed redescription, with designation of a neotype forChrysaora chesapeakei, and clarify the description ofChrysaora quinquecirrha. Since CaribbeanChrysaoraare genetically similar toChrysaora chesapeakei, we provisionally term themChrysaorac.f.chesapeakei. The presence ofMawia benovicioff the coast of Western Africa provides a potential source region for jellyfish introduced into the Adriatic Sea in 2013.