Neotenous origins for pelagic octopuses

The 'ctenoglossans' are an enigmatic group of transparent, pelagic octopuses that spend their entire life without touching the seafloor. Molecular and morphological evidence shows that the ctenoglossans have arisen via neoteny, the persistence of larval attributes in the adult form. The ctenoglossans have evolved from the planktonic early-dispersal stages of familiar benthic octopuses. Extreme adaptations of this group to their midwater habitat have masked their origins. The general appearance of the ctenoglossans is strikingly similar to that of non-octopod midwater cephalopods, the Glass Squids (family Cranchiidae). The Ctenoglossa include three families: the Glass Octopus (Family Vitreledonellidae, Figure 1A), Telescope Octopus (Family Amphitretidae, Figure 1B), and members of the family Bolitaenidae (Figures 1C,D). These octopuses live in tropical and temperate waters worldwide and possess many adaptations to their pelagic lifestyle, such as a transparent body, reduced organ size, modified eyes and in certain taxa large, simple chromatophores and light-producing organs. These adaptations have complicated morphological analyses and obscured the phylogenetic relationships of this group within the Octopoda [1,2]. Naef proposed that the Ctenoglossa diverged from all other octopods in the Upper Cretaceous [1]. Voight proposed that the Ctenoglossa were polyphyletic, with the Bolitaenidae placed as the sister group to all remaining incirrate octopuses, while the Amphitretidae and Vitreledonellidae were grouped with the shelled argonauts and their relatives (superfamily Argonautoidea) [3]. To investigate the origins of the ctenoglossan octopuses, we amplified a total of 3400 base pairs (bp) of DNA from the Vampire squid and 17 species of Octopoda, including three species from the ctenoglossan families Vitreledonellidae and Bolitaenidae. Sequences from three mitochondrial (12S rDNA, 16S rDNA, cytochrome oxidase I) and three nuclear (rhodopsin, octopine dehydrogenase, pax-6) genes were used in maximum likelihood (ML) and Bayesian analyses (Supplemental Data). The phylogenetic tree for the concatenated dataset (Figure 1E) reveals that the ctenoglossans are more closely related to benthic octopuses than previously suspected. The closest sister taxa are members of the family Octopodidae, namely the Antarctic genus Pareledone (Figure 1F); the second nearest is the deep-water genus Graneledone. In contrast to the entirely pelagic ctenoglossans, members of both these genera have a wholly benthic lifestyle and large benthic hatchlings [4]. The distribution of the ctenoglossans in tropical and temperate waters contrasts with that of their closest relative, Pareledone, which is restricted to Antarctic waters. This geographic separation suggests that these groups diverged prior to the establishment of the Circum-Antarctic Current, about 33.5 million …