Evolution of development type in benthic octopuses: holobenthic or pelago-benthic ancestor?

Abstract

Octopuses of the family Octopodidae are singular among cephalopods in their reproductive behavior, showing two major reproductive strategies: the first is the production of few and large eggs resulting in well-developed benthic hatchlings (holobenthic life history); the second strategy is the production of numerous small eggs resulting in freeswimming planktonic hatchlings (pelago-benthic life history). Here, we utilize a Bayesian-based phylogenetic comparative method using a robust molecular phylogeny of 59 octopus species to reconstruct the ancestral states of development type in benthic octopuses, through the estimation of the most recent common ancestors and the rate of gain and loss in complexity (i.e., planktonic larvae) during the evolution. Wefound a high probability that a free-swimming hatchling was the ancestral state in benthic octopuses, and a similar rate of gain and loss of planktonic larvae through evolution. These results suggest that in benthic octopuses the holobenthic strategy has evolved from an ancestral pelago-benthic life history. During evolution, the paralarval stage was reduced to well-developed benthic hatchlings, which supports a ‘‘larva-first’’ hypothesis. We propose that the origin of the holobenthic life history in benthic octopuses is associated with colonization of cold and deep sea waters.