Comparative analysis of chromosome counts infers three paleopolyploidies in the mollusca

Abstract

The study of paleopolyploidies requires the comparison of multiple whole genome sequences. If the branches of a phylogeny on which a whole-genome duplication (WGD) occurred could be identified before genome sequencing, taxa could be selected that provided a better assessment of that genome duplication. Here, we describe a likelihood model in which the number of chromosomes in a genome evolves according to a Markov process with one rate of chromosome duplication and loss that is proportional to the number of chromosomes in the genome and another stochastic rate at which every chromosome in the genome could duplicate in a single event. We compare the maximum likelihoods of a model in which the genome duplication rate varies to one in which it is fixed at zero using the Akaike information criterion, to determine if a model with WGDs is a good fit for the data. Once it has been determined that the data does fit the WGD model, we infer the phylogenetic position of paleopolyploidies by calculating the posterior probability that a WGD occurred on each branch of the taxon tree. Here, we apply this model to a molluscan tree represented by 124 taxa and infer three putative WGD events. In the Gastropoda, we identify a single branch within the Hypsogastropoda and one of two branches at the base of the Stylommatophora. We also identify one or two branches near the base of the Cephalopoda.

FIG. 1.—

An ideal sampling of three taxa for investigating the genome duplication indicated by the dash. By selecting one taxon each from clades A, B, and C, the investigator would minimize the amount of shared history either before or after the event and thus have the best chance of accurately reconstructing the effects of the duplication on the genome.

FIG. 2.—

(a) The cladogram of the Mollusca used in this study. Several clades important to this study are identified with brackets. (b) The phylogeny of molluscan taxa used in this study. The topology of this tree is the same as the tree in (a), but here branch lengths are shown in millions of years as derived from the fossil record using the Paleobiology Database. Zero length branches are shown as polytomies.

FIG. 3.—

The AIC for each of three models of chromosome number evolution in extant mollusc families. Each figure shows the AICs for all three models conditioned on the number of chromosomes found in the last common ancestor of all Mollusca for a given set of branch lengths.

FIG. 4.—

The phylogeny of all the terminal taxa in the Hypsogastropoda using the branch lengths from Tree-10⁶ showing the posterior probability of a WGD on each branch. The Capulidae–Neogastropoda branch is marked, as it has a very high posterior probability of a WGD for all sets of branch lengths, whereas all the other branches have essentially none.

FIG. 5.—

Posterior probabilities for a WGD on two branches near the base of the Stylommatophora. (a) The phylogeny of all the terminal taxa in a clade containing the Stylommatophora, the Systellommatophora, and the Ellobiidae using the branch lengths from Tree-10⁶ showing the posterior probability of a WGD on each branch. The Stylommatophora branch and the Sigmurethra–Orthurethra branch are marked, as they have a relatively high posterior probability of a WGD, whereas all the other branches have essentially none. (b) A bar plot showing the posterior probability of a WGD on either of these branches as well as on each of these branches individually under each of the three different sets of branch lengths.

FIG. 6.—

Posterior probabilities for a WGD on branches within the Cephalopoda. (a) The phylogeny of all the terminal taxa in the Cephalopoda with Gastropoda and Scaphopoda included as an outgroup using the branch lengths from Tree-10⁶ showing the posterior probability of a WGD on each branch. Two branches with relatively high posterior probability of a WGD are labeled above the branch. (b) A bar plot showing the posterior probability of a WGD on various branches in the phylogeny. The dark bars show the posterior probability of a WGD on the specified branch or branches. The light bars show the posterior probability that there were WGDs on any pair of branches in the Cephalopoda including the specified branch or branches. The posterior probability is shown by the large bar for Tree-10⁵, by the lower error bar for Tree-10⁴, and by the upper error bar for Tree-10⁶.