Evolution of box jellyfish (Cnidaria: Cubozoa), a group of highly toxic invertebrates

Abstract

Cubozoa (Cnidaria: Medusozoa) represents a small clade of approximately 50 described species, some of which cause serious human envenomations. Our understanding of the evolutionary history of Cubozoa has been limited by the lack of a sound phylogenetic hypothesis for the group. Here, we present a comprehensive cubozoan phylogeny based on ribosomal genes coding for near-complete nuclear 18S (small subunit) and 28S (large subunit) and partial mitochondrial 16S. We discuss the implications of this phylogeny for our understanding of cubozoan venom evolution, biogeography and life-history evolution. Our phylogenetic hypothesis suggests that: (i) the last common ancestor of Carybdeida probably possessed the mechanism(s) underlying Irukandji syndrome, (ii) deep divergences between Atlantic and Indo-Pacific clades may be explained by ancient vicariant events, and (iii) sexual dimorphism evolved a single time in concert with complex sexual behaviour. Furthermore, several cubozoan taxa are either para-or polyphyletic, and we address some of these taxonomic issues by designating a new family, Carukiidae, a new genus, Copula, and by redefining the families Tamoyidae and Tripedaliidae. Lastly, cubozoan species identities have long been misunderstood and the data presented here support many of the recent scientific descriptions of cubozoan species. However, the results of a phylogeographic analysis of Alatina moseri from Hawai'i and Alatina mordens from Australia indicate that these two nominal species represent a single species that has maintained metapopulation cohesion by natural or anthropogenic dispersal.

Recognition of the Californian cubozoan population as a new species—<i>Carybdea confusa</i> n. sp. (Cnidaria, Cubozoa, Carybdeida)

“…In Mayer s (1910: p. 507) opinion the most characteristic features for specific distinction are the shape and size of the pedalia and the number and character (branched or unbranched) of the velar canals . Therefore, species were first established and later on renamed or regrouped and vice versa as in the cases of Carybdea arborifera (Maas 1897, 1903, Mayer 1906, Mayer 1910, Bentlage et al 2010, Crow et al 2015, Carybdea xaymacana Conant, 1897(Conant 1897, Bigelow 1938, Studebaker 1972 and Alatina alata (Reynaud, 1830) (Reynaud 1830, Mayer 1906, Gershwin 2005a,b, Bentlage et al 2010, Lewis et al 2013. Such changes occurred because in the opinion of the leading scientists of the first half of the 20 th century, the biodiversity of the genus Carybdea was less numerous than indicated by Haeckel (1880) and should had been reduced to one, two or maximally three species, Carybdea alata, Carybdea marsupialis and/or Carybdea rastonii, depending on the author (Maas 1897, 1903, Bigelow 1909, 1938, Mayer 1910, Stiasny 1919, Thiel 1928, 1936, Kramp 1961).…”

“…Larson & Arneson (1990) observed specimens of Carybdea rastonii from South Australia and found fewer similarities between the Australian and Californian specimens than between the Caribbean and Californian specimens and followed the trend of several publications that classified carybdeid populations from many different locations as Carybdea marsupialis (Mayer 1910, Bigelow 1938, Kramp 1961, Studebaker 1972, Cutress & Studebaker 1972, Kazmi & Sultana 2008. Several authors did not agree with this reclassification of carybdeid specimens from California, Hawaii and the Caribbean to Carybdea marsupialis as the morphological characters did not fit (Fenner 1997, communication with George I. Matsumoto cited in Fenner 1997, Gershwin 2005a, and even the molecular characters hinted they belonged to a different-to-Carybdea marsupialis (Linnaeus, 1758) species (Collins 2002, Gershwin 2005a, Bentlage et al 2010.…”

“…Campbell (1974: 142) stated that gonads in most cnidarians are not separate organs, as found in higher animals, because germ cells are generally found in the interstitial portions of the body tissue which, prior to the formation of germ cells, exhibit no reproductive specialization. However, we follow Campbell (1974), Marques & Collins (2004), Bentlage et al (2010), Morandini & Marques (2010), Straehler-Pohl & Toshino (2015) and Straehler-Pohl & Gul (2016) in using the term gonads to refer to areas where gametes are formed.…”

First records ofCarybdea marsupialisproliferation (Cnidaria: Cubozoa) along the eastern Tunisian coast (Central Mediterranean)

“…Within the Carybdeidae family, Carybdea Péron & Lesueur, 1809 is the sole genus recognized, with 7-8 accepted species (Bentlage et al 2010;Bentlage & Lewis 2012), including the oldest described cubozoan taxon Carybdea marsupialis (Linneaus, 1758), C. murrayana (Haeckel, 1880), C. rastonii (Haacke, 1887), C. brevipedalia (Kishinouye, 1891), C. arborifera (Mass, 1897), C. xaymacana (Conant, 1897), C. branchi (Gershwin & Gibbons, 2009) and, more recently, C. morandinii (Straehler-Pohl & Jarms, 2005), whose validity has still to be confirmed. Cubozoan jellyfish, including C. marsupialis, have a biphasic life cycle with a benthic polyp and a free-swimming medusa.…”

Internal fertilization and sperm storage in cnidarians: a response to Orr and Brennan

“…While their plesiomorphic reproductive mode is external fertilization (e.g., in Chironex fleckeri) [5], there is evidence for an evolutionary transformation to the derived strategy of internal fertilization [6]. Cubozoan species such as the carybdeid Carybdea marsupialis and the alatinid Alatina alata are ovoviviparous, a reproductive mode in which ova are internally fertilized by sperm taken up by the female medusae during spawning aggregations with males [7].…”