Correlated Evolution between Mode of Larval Development and Habitat in Muricid Gastropods

<div><p>Abstract</p><p>Larval modes of development affect evolutionary processes and influence the distribution of marine invertebrates in the ocean. The decrease in pelagic development toward higher latitudes is one of the patterns of distribution most frequently discussed in marine organisms (Thorson's rule), which has been related to increased larval mortality associated with long pelagic durations in colder waters. However, the type of substrate occupied by adults has been suggested to influence the generality of the latitudinal patterns in larval development. To help understand how the environment affects the evolution of larval types we evaluated the association between larval development and habitat using gastropods of the Muricidae family as a model group. To achieve this goal, we collected information on latitudinal distribution, sea water temperature, larval development and type of substrate occupied by adults. We constructed a molecular phylogeny for 45 species of muricids to estimate the ancestral character states and to assess the relationship between traits using comparative methods in a Bayesian framework. Our results showed high probability for a common ancestor of the muricids with nonpelagic (and nonfeeding) development, that lived in hard bottoms and cold temperatures. From this ancestor, a pelagic feeding larva evolved three times, and some species shifted to warmer temperatures or sand bottoms. The evolution of larval development was not independent of habitat; the most probable evolutionary route reconstructed in the analysis of correlated evolution showed that type of larval development may change in soft bottoms but in hard bottoms this change is highly unlikely. Lower sea water temperatures were associated with nonpelagic modes of development, supporting Thorson's rule. We show how environmental pressures can favor a particular mode of larval development or transitions between larval modes and discuss the reacquisition of feeding larva in muricids gastropods.</p></div

Estimated parameters of the phylogenetic logistic regressions performed to assess the effects of sea water temperature on the presence of pelagic stage or feeding larva in muricid gastropods.

<p>The response variable was coded as 0: present, 1: absent. Phylogenetic logistic regression with Firth correction using the function PLogReg.m <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094104#pone.0094104-Ives1" target="_blank">[46]</a> created for Matlab. Parameter estimates for phylogenetic signal (<i>a</i>) and for the regression coefficients (<i>b₀, b₁</i>). P-values lower than 0.05 indicated in bold. Bootstrapping was performed by simulating 2000 data sets.</p

Reconstruction of the ancestral state of mode of larval development and the type of substrate occupied by muricid gastropods.

<p>Reconstruction was made using the most recent common ancestor approach <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094104#pone.0094104-Pagel1" target="_blank">[25]</a>, based on the topology and branch length obtained in the sample of trees. The posterior probability of occurrence of each state is represented in the main nodes. Larval development is classified as direct, direct with nurse eggs, lecithotrophic with nurse eggs and planktotrophic; the type of substrate is classified as soft or hard. The character states present in extant species are represented in the tips of the tree. The name of Muricids subfamilies are indicated in each clade except for the two subfamilies with only one species included in our study (<i>Vitularia salebrosa</i>, Muricopsinae; <i>Trophon geversianus</i>, Trophoninae).</p

Evolutionary pathways and rates coefficients of the model of dependent evolution between larval development and type of substrate occupied by adults.

<p>A) Flow diagram describing evolution between each possible combination of larval stage and type of substrate (transition rates are represented proportional to the average values), B) Posterior distributions of the rate coefficients of the model. The plots are arranged so that vertical pairs correspond to rates that must be the same for the independent model to be true <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094104#pone.0094104-Pagel7" target="_blank">[45]</a>. Z indicates the proportion of time the rates are assigned to zero.</p

Posterior probabilities of the ancestral state reconstruction of traits in the nodes that give rise to the principal subfamilies of muricid gastropods.

<p>Traits analyzed were mode of larval development (NE: nurse eggs), type of development coded as presence of pelagic or feeding larva, and type of substrate occupied by adults (soft or hard bottoms). Posterior probability of occurrence of traits is indicated ± standard error; with the higher values for a given trait indicated in bold.</p

Relationship between temperature and type of larval development.

<p>The box plots show the sea water temperature associated with each mode of larval development for pelagic stage (light gray) and feeding type (darkgray). The horizontal band indicates the median, the bottom and top of the box delimit the first and third quartiles and the whiskers point the values within 1.5 times the interquartile.</p

Phylogenetic signal for mode of larval development in muricid gastropods.

<p>Mode of larval development (NE: nurse eggs), type of development coded as presence of pelagic or feeding larva, and type of substrate occupied by adults estimated using Bayesian Tip-association Significance testing software (BaTS) <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094104#pone.0094104-Pagel5" target="_blank">[41]</a>. AI: association index; PS: parsimony score; MC: monophyletic clade size statistic; HPD CIs highest posterior density confidence intervals. P-values from the BaTS null hypothesis test lower than 0.05 indicated in bold.</p

Latitudinal distribution of modes of larval development.

<p>The latitudinal distribution for species with planktotrophic larvae (blue), lecithotrophic larvae (purple) and direct development (green) is shown using vertical lines from the northern to the southern point of distribution reported in the literature. The panels show the species included in the phylogenetic (upper) and all the species present in our database (lower).</p

Parameters that describe the models of evolution analyzed for latitude and sea water temperature in muricid gastropods and criterion for selection.

<p>The high probability distribution for parameters alpha and beta is shown within brackets. The selection of evolutionary models that best fit the evolution of the variables was made by Bayes Factors implemented in Tracer v.1.5 software <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094104#pone.0094104-Rambaut1" target="_blank">[36]</a>. Asterisks indicate the models selected.</p

Pagel's [39],[44] scaling parameters for latitude and sea water temperature in muricid gastropods and criterion for selection.

<p>Parameters were selected using the Bayes Factor (BF) implemented in Tracer v.1.5 software <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094104#pone.0094104-Rambaut1" target="_blank">[36]</a>. Asterisks indicate the models selected.</p