Deep-sea mystery solved: astonishing larval transformations and extreme sexual dimorphism unite three fish families

Abstract

The oceanic bathypelagic realm (1000–4000 m) is a nutrient-poor habitat. Most fishes living there have pelagic larvae using the rich waters of the upper 200 m. Morphological and behavioural specializations necessary to occupy such contrasting environments have resulted in remarkable developmental changes and life-history strategies. We resolve a long-standing biological and taxonomic conundrum by documenting the most extreme example of ontogenetic metamorphoses and sexual dimorphism in vertebrates. Based on morphology and mitogenomic sequence data, we show that fishes currently assigned to three families with greatly differing morphologies, Mirapinnidae (tapetails), Megalomycteridae (bignose fishes) and Cetomimidae (whalefishes), are larvae, males and females, respectively, of a single family Cetomimidae. Morphological transformations involve dramatic changes in the skeleton, most spectacularly in the head, and are correlated with distinctly different feeding mechanisms. Larvae have small, upturned mouths and gorge on copepods. Females have huge gapes with long, horizontal jaws and specialized gill arches allowing them to capture larger prey. Males cease feeding, lose their stomach and oesophagus, and apparently convert the energy from the bolus of copepods found in all transforming males to a massive liver that supports them throughout adult life.

Species are hypotheses: avoid connectivity assessments based on pillars of sand

“…In extreme cases, different life-history stages or sexes can wrongly be attributed to different taxa (e.g. Johnson et al 2009), confounding estimates of connectivity. When the different sexes or stages inhabit different environments such as different depths, estimating dispersal from a single life stage or sex can bias interpretation of connectivity patterns but also taxonomic interpretations (Box 1).…”

“…First, the state of the art of taxonomy may be so preliminary that different life stages of a single organism might have been erroneously classified as different species or even families (e.g. Johnson et al 2009). Second, the evidence that two evolutionary lineages are engaged in definitive divergence may not be easy to evaluate when the split between the emergent lineages is recent (the 'grey zone' of de Queiroz 1998).…”

Taxonomy and systematics of larval Indo-Pacific fishes: a review of progress since 1981

“…Not until 1991 did R. K. Johnson and E. Bertelsen publish the definitive morphological evidence documenting the remarkable ontogenetic changes that remodel the 'rosaura' larva into the highly specialized giganturid adult form. In 2009, G. D. Johnson and coworkers (Johnson et al 2009) documented the ''most extreme example of ontogenetic metamorphoses and sexual dimorphism in vertebrates'' when they showed that fishes then assigned to three families with very different morphologies-Mirapinnidae, Megalomycteridae and Cetomimidae-were larvae, males and females, respectively, of one family. The Mirapinnidae, described as a new order in 1956 (Bertelsen and Marshall 1956), lacks scales and lateral lines, but has a large mouth with almost vertically oriented jaws and, in most individuals, a long ribbon-like streamer formed from the skin of the caudal fin.…”

Different on the inside: extreme swimbladder sexual dimorphism in the South Asian torrent minnows

“…Sexual dimorphism in fishes most commonly involves external features that play a role during reproductive behaviour and that range from variably sized fins [14,15], teeth and/or jaws [16,17] in males to extreme differences in body size [18] and/or shape [19] between the sexes. Sexual dimorphism of internal organs other than the gonads is rare, not only among fishes, but also in other groups of vertebrates, and is limited to a few examples, including (but not restricted to) the sexually dimorphic kidney of sticklebacks [20], salamanders [21] and squamates [22] and the larynx in vocal tetrapods [23].…”