A multi-gene phylogeny of Cephalopoda supports convergent morphological evolution in association with multiple habitat shifts in the marine environment

Abstract

BackgroundThe marine environment is comprised of numerous divergent organisms living under similar selective pressures, often resulting in the evolution of convergent structures such as the fusiform body shape of pelagic squids, fishes, and some marine mammals. However, little is known about the frequency of, and circumstances leading to, convergent evolution in the open ocean. Here, we present a comparative study of the molluscan class Cephalopoda, a marine group known to occupy habitats from the intertidal to the deep sea. Several lineages bear features that may coincide with a benthic or pelagic existence, making this a valuable group for testing hypotheses of correlated evolution. To test for convergence and correlation, we generate the most taxonomically comprehensive multi-gene phylogeny of cephalopods to date. We then create a character matrix of habitat type and morphological characters, which we use to infer ancestral character states and test for correlation between habitat and morphology.ResultsOur study utilizes a taxonomically well-sampled phylogeny to show convergent evolution in all six morphological characters we analyzed. Three of these characters also correlate with habitat. The presence of an autogenic photophore (those relying upon autonomous enzymatic light reactions) is correlated with a pelagic habitat, while the cornea and accessory nidamental gland correlate with a benthic lifestyle. Here, we present the first statistical tests for correlation between convergent traits and habitat in cephalopods to better understand the evolutionary history of characters that are adaptive in benthic or pelagic environments, respectively.DiscussionOur study supports the hypothesis that habitat has influenced convergent evolution in the marine environment: benthic organisms tend to exhibit similar characteristics that confer protection from invasion by other benthic taxa, while pelagic organisms possess features that facilitate crypsis and communication in an environment lacking physical refuges. Features that have originated multiple times in distantly related lineages are likely adaptive for the organisms inhabiting a particular environment: studying the frequency and evolutionary history of such convergent characters can increase understanding of the underlying forces driving ecological and evolutionary transitions in the marine environment.

Predictable transcriptome evolution in the convergent and complex bioluminescent organs of squid

“…We scored species as present or absent for bacterial photophores (summarized in ref. 25). We estimated ancestral character states using the ML topology under parsimony in Mesquite (51) and under a two-rate Markov model in the R package "corHMM" (52).…”

“…The ANG consists of a cluster of tubules housing a consortium of bacteria, and was very likely present in the common ancestor of squid (25,29,30). The microscopic anatomy, ontogenetic and bacteriogenic properties of the photophore bear striking similarities to those of the ANG (20,31).…”

“…Bacterial photophores of squid are evolutionary novelties that may have arisen separately in two squid clades (6,7,25), but the details of these evolutionary origins have remained obscure. Although many novelties evolve by modifications to existing structures-such as fishes' electric organs, which are probably modified muscles-bacterial photophores are not obviously related to any structure in nonluminescent squid that might represent a single, direct evolutionary precursor.…”

The evolution of jaw protrusion mechanics has been tightly coupled to bentho-pelagic divergence in damselfishes (Pomacentridae)

“…One of the most common patterns of evolution among aquatic animals is transitioning between feeding niches that lie at different points along this bentho-pelagic niche axis, and such diversification has arisen repeatedly in molluscs, crustaceans, annelids, pinnipeds, elasmobranchs and bony fishes (Bracken et al, 2009;Cooper et al, 2010;Jones et al, 2013;Lindgren et al, 2012;Regier et al, 2010;Struck et al, 2015;Wilga et al, 2007).…”

Macroevolution and Paleobiogeography of Jurassic-Cretaceous Ammonoids

“…Typically, the homeomorphic traits are restricted to adult forms, so homeomorphs can be distinguished by considering their entire ontogeny (Donovan et al 1981). It should also be noted that modern coleoid cephalopods show extensive convergent evolution as well (Lindgren et al 2012).…”