Mesozoic origin of coleoid cephalopods and their abrupt shifts of diversification patterns.

Coleoids are the most diverse group of cephalopod mollusks. While their origin is date during the Mesozoic, the diversification pattern is unknown. However, two hypotheses have been proposed. The first suggests an increasing diversification rate after the Cretaceous-Paleogene extinction event (K-Pg) as consequence of empty habitats left by the ammonites and belemnites. The second hypothesis proposes a mid-Cenozoic increase in diversification rate related to distributional changes during ice ages and biotic interactions. To test these hypotheses, we estimated a lineage through time (LTT) and the gamma-statistic along with model-based diversification rates. These analyses were conducted on a dated molecular phylogeny for coleoids that we reconstructed using five molecular markers (cytochrome b, 16S rRNA, cytochrome oxidase I, rhodopsin, and PAX-6). Our divergence time estimation suggests that coleoids originated in the Mesozoic Era (Middle Triassic) and that both main clades (Decapodiformes and Octopodiformes) diverged in the Cretaceous/Jurassic Period. The LTT, gamma statistic, and diversification rates inferred with the Bayesian Analysis of Macro-evolutionary Mixtures (BAMM), indicate an acceleration in diversification rate over time since the origin of coleoids. Additionally, BAMM allowed us to detect abrupt increases in diversification rate before and after the K-Pg boundary. Our results partially support both hypotheses as all analyses indicate that the coleoid diversification rate was increasing during the Cenozoic. However, our results also indicate increasing diversification rates before the K-Pg boundary. We propose that the radiation of coleoids has been shaped by an acceleration in diversification rate over time, including exceptional episodes of abrupt increases before and after the K-Pg boundary.

A phylogenetic approach to understand the evolution of reproduction in coleoid cephalopods.

A central question in the evolution of life-histories is whether organisms reproduce once or repeatedly. For cephalopods, the main differences between semelparous and iteroparous are based on ovulation pattern and spawning type. The different reproductive strategies in coleoid cephalopods could be related to the habitat in which the species dwell (coastal vs. oceanic) and/or to environmental forces, thus, both aspects should be quantitatively evaluated under an evolutionary perspective to reconstruct: (a) the ancestral ovulation type of coleoid cephalopods, and (b) the potential of correlated evolution between ovulation type versus habitat and environment. Ancestral states of ovulation type were estimated using stochastic mapping based on literature data (i.e. synchronous or asynchronous), and this information was combined with a new molecular phylogeny including 165 species. The evolutionary correlation between ovulation type, habitat, and environment was estimated by means of the Markov model comparing the rates of gain and loss. The estimates of ancestral states of ovulation type for coleoid cephalopods resulted in a high probability that Octopodiformes evolved from synchronous ovulation type, and Decapodiformes from asynchronous ovulation type. The three traits evaluated presented phylogenetic signal, although no correlation was found between habitat and ovulation type. Overall, species in stable environments showed a tendency towards synchronous ovulation type, while the asynchronous ovulation pattern was found more frequently in species that live in unstable environments, being this last trait also responsible for triggering the change of ovulation type in some species throughout evolution.

Updated molecular phylogeny of the squid family Ommastrephidae: Insights into the evolution of spawning strategies.

Two types of spawning strategy have been described for ommastrephid squids: coastal and oceanic. It has been suggested that ancestral ommastrephids inhabited coastal waters and expanded their distribution into the open ocean during global changes in ocean circulation in the Oligocene. This hypothesis could explain the different reproductive strategies in oceanic squids, but has never been tested in a phylogenetic context. In the present study, we assess the coastal-to-open-ocean hypothesis through inferring the evolution of reproductive traits (spawning type) of ommastrephid squids using the phylogenetic comparative method to estimate ancestral states and divergence times. This analysis was performed using a robust molecular phylogeny with three mitochondrial genes (COI, CYTB and 16S) and two nuclear genes (RHO and 18S) for nearly all species of ommastrephid squid. Our results support dividing the Ommastrephidae into the three traditional subfamilies, plus the monotypic subfamily Todaropsinae as proposed previously. Divergence times were found to be older than those suggested. Our analyses strongly suggest that early ommastrephid squids spawned in coastal areas, with some species subsequently switching to spawn in oceanic areas, supporting previous non-tested hypotheses. We found evidence of gradual evolution change of spawning type in ommastrephid squids estimated to have occurred since the Cretaceous.

Sexual Selection and the Evolution of Male Reproductive Traits in Benthic Octopuses.

Competition between same-sex organisms, or intra-sexual selection, can occur before and after mating, and include processes such as sperm competition and cryptic female choice. One of the consequences of intra-sexual selection is that male reproductive traits tend to evolve and diverge at high rates. In benthic octopuses, females often mate with more than one male in a single reproductive event, opening the venue for intra-sexual selection at multiple levels. For instance, males transfer spermatophores through hectocotylus, and can remove the spermatophores left by other males. Considering the limited evidence on post-copula competition in benthic octopuses, and the potential to affect the evolution of reproductive traits within octopodids, we put this hypothesis to a test employing a phylogenetic comparative approach. We combined data on hectocotylized arm length (HAL), ligula length (LL), spermatophore length (SL) with a Bayesian molecular phylogeny of 87 species, to analyze how reproductive traits have diverged across lineages and covary with body size (mantle length; ML). First, additionally to ML, we estimated the phylogenetic signal (λ) and mode of evolution (κ) in each reproductive trait. Second, we performed phylogenetic regressions to quantify the association among reproductive traits and their co-variation with ML. This analysis allowed us to estimate the phenotypic change along a branch into the phylogeny, and whether selection may have played a role in the evolution and diversification of specific clades. Estimations of λ were always high (>0.75), indicating concordance between the traits and the topology of the phylogenetic tree. Low values of κ (<1.0) suggested that evolution depends on branch lengths. All reproductive traits exhibiting a positive relation with ML (ß > 0.5 in all cases). Overall, evolutionary rate models applied to the SL-ML regression suggested that octopuses of the family Megaleledonidae have evolved larger spermatophores than expected for their size. The regression HAL-ML indicated that HAL was more variable in Megaleledonidae than in the remaining clades, suggesting that the high divergence across species within this group might partially reflect intra-sexual selection. These results support the hypothesis that, at least in some lineages, sexual selection may account for the divergence in reproductive traits of male octopuses.

Environmental and ecological factors mediate taxonomic composition and body size of polyplacophoran assemblages along the Peruvian Province.

Intertidal communities' composition and diversity usually exhibit strong changes in relation to environmental gradients at different biogeographical scales. This study represents the first comprehensive diversity and composition description of polyplacophoran assemblages along the Peruvian Province (SE Pacific, 12°S-39°S), as a model system for ecological latitudinal gradients. A total of 4,775 chitons from 21 species were collected on twelve localities along the Peruvian Province. This sampling allowed us to quantitatively estimate the relative abundance of the species in this assemblage, and to test whether chitons conform to elementary predictions of major biogeographic patterns such as a latitudinal diversity gradient. We found that the species composition supported the division of the province into three ecoregional faunal groups (i.e. Humboldtian, Central Chile, and Araucanian). Though chiton diversity did not follow a clear latitudinal gradient, changes in species composition were dominated by smaller scale variability in salinity and temperature. Body size significantly differed by ecoregions and species, indicating latitudinal size-structure assamblages. In some localities body size ratios differed from a random assemblage, evidencing competition at local scale. Changes in composition between ecoregions influence body size structure, and their overlapping produce vertical size segregation, suggesting that competition coupled with environmental conditions structure these assemblages.

Thorson's rule, life-history evolution, and diversification of benthic octopuses (Cephalopoda: Octopodoidea).

Here, we evaluate the so-called Thorson's rule, which posits that direct-development and larger eggs are favored toward the poles in marine organisms and whose validity been the subject of considerable debate in the literature, combining an expanded phenotypic dataset encompassing 60 species of benthic octopuses with a new molecular phylogeny. Phylogenetic reconstruction shows two clades: clade 1 including species of the families Eledonidae, Megaleledonidae, Bathypolypodidae, and Enteroctopodidae, and clade 2 including species of Octopodidae. Egg size, development mode, and all environmental variables exhibited phylogenetic signal, partly due to differences between the two clades: whereas most species in clade 1 inhabit cold and deep waters, exhibit large eggs and hatchling with holobenthic development, species from clade 2 inhabit tropical-temperate and shallow waters, evolved small eggs, and generally exhibit merobenthic development. Phylogenetic regressions show that egg size exhibits a conspicuous latitudinal cline, and that both egg size and development mode vary with water temperature. Additionally, analyses suggest that egg size is constrained by body size in lineages with holobenthic development. Taken together, results suggest that the variation in egg size and development mode across benthic octopuses is adaptive and associated with water temperature, supporting Thorson's rule in these organisms.