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

Artículo de publicación ISIOctopuses 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.This work was partially funded by grants to C.I. FONDECYT 3110152 and to E.P. ICM P05-002 and PFB-23. Support to M.C. Pardo-Gandarillas by a MECESUPChil

AMOVA for all species.

<p>Percentage of variation explained among groups north and south of 30°S, among populations within groups, and within populations are shown.</p><p>Values in bold indicate association to significant AMOVA’s Φ-statistics.</p

Box-plots of global (a and b) and per population (c and d) haplotype (a and c) and nucleotide (b and d) diversities for high and low dispersers.

<p>Box-plots of global (a and b) and per population (c and d) haplotype (a and c) and nucleotide (b and d) diversities for high and low dispersers.</p

Map of the study area along the coast of Chile indicating the sampling sites and the sample size per site for each of the analyzed species.

<p>Map of the study area along the coast of Chile indicating the sampling sites and the sample size per site for each of the analyzed species.</p

GLMMs performed to compare genetic structure in species with high and low dispersal potential and biogeographic regions (north and south of 30°S), with respect to haplotype diversity, nucleotide diversity, number of substitutions, and genetic differentiation (global Φ_ST).

<p>Species were nested to dispersal in the models. For each model the AIC value is shown and the variance estimate of fixed effects (Estimate), standard error, degrees of freedom (<i>df</i>), t-value ratio and <i>P</i> values of the intercept and of the contributions of dispersal potential (DP), biogeographic region (BR) (for genetic diversities and number of substitutions) or biogeographic differentiation (BD) (for genetic differentiation), and the interaction of DP x BR and DP x BD for diversities and differentiation, respectively.</p><p>Significant values are in bold (<i>P</i><0.05).</p

Species analyzed and the corresponding depth range in meters that they inhabit, and dispersal potential (DP) as number of days that larvae spend in the water column.

<p>*Considered as low dispersers in this study.</p

Latitudinal range analyzed in degrees for each species (Lat); number of localities (NL); number of sequences analyzed per species (NS); length of final truncated alignment (LA); percentage of variable sites (%V); average haplotype (h) and nucleotide (π) diversities; S_nn; global Φ_ST, and Mantel correlation coefficient (MCC).

<p>Significant values are in bold.</p

Estimates of migration rates (<i>m</i>) in each direction across 30°S, time of divergence (<i>t</i>) between biogeographic regions, and genetic diversities (Θ) (north = Θ_N; south = Θ_S; ancestral = Θ_A), based on the isolation-with-migration model implemented in IMa2.

<p>For each parameter per species, the high point (HP) and 95% highest posterior density (95% HPD) of the marginal posterior probabilities are shown. Significant m values of the LRT are denoted with asterisks; *<i>P</i><0.05, **<i>P</i><0.01, ***P<0.001. <i>t</i> was scaled using substitution rates of 2% and 10% per million years, <i>t</i> 2% and <i>t</i> 10% respectively as is expressed in thousands of years (Kyr).</p><p>Significant values are in bold.</p

GLMMs performed to compare species with high and low dispersal potential (DP) in AMOVA’s F statistics among groups (Φ<i>_CT</i>), among populations within groups (Φ<i>_SC</i>), and within populations (Φ<i>_ST</i>).

<p>Species were nested to dispersal in the model. For each model the AIC value, and the variance estimate of fixed effects (Estimate), standard error, degrees of freedom (<i>df</i>), t-value ratio and <i>P</i> values of the intercept are shown.</p><p>Significant values are in bold (<i>P</i><0.05).</p

Isolation-with-migration analysis of four species with significant structure across the 30°S biogeographic break.

<p>(a) Marginal posterior probability distribution of migration rate estimates in each direction for each species. (b) Estimated Θ (2 Ne) values for each biogeographic region (north and south) as well as the ancestral Θ against genetic differentiation (global Φ_ST). Asterisks denote estimated Θ 95% HPD that do not overlap with either ancestral Θ or the estimated Θ in the other biogeographic region. (c) Marginal posterior probability distributions of divergence time (<i>t</i>) estimates expressed in thousands of years (Kyr). Divergence time estimates were scaled using 2% and 10% per million year substitution rates. (d) Highest probability value of estimated migration rates (<i>m</i>) in each direction, and divergence times (<i>t</i>) expressed in thousands of years (Kyr) scaled using 2% per million year substitution rate, versus genetic differentiation (global Φ_ST). Asterisks indicate significant values based on the likelihood ratio test.</p