Phylogenomic resolution of the root of Panpulmonata, a hyperdiverse radiation of gastropods: new insight into the evolution of air breathing.

Transitions to terrestriality have been associated with major animal radiations including land snails and slugs in Stylommatophora (>20 000 described species), the most successful lineage of 'pulmonates' (a non-monophyletic assemblage of air-breathing gastropods). However, phylogenomic studies have failed to robustly resolve relationships among traditional pulmonates and affiliated marine lineages that comprise clade Panpulmonata (Mollusca, Gastropoda), especially two key taxa: Sacoglossa, a group including photosynthetic sea slugs, and Siphonarioidea, intertidal limpet-like snails with a non-contractile pneumostome (narrow opening to a vascularized pallial cavity). To clarify the evolutionary history of the panpulmonate radiation, we performed phylogenomic analyses on datasets of up to 1160 nuclear protein-coding genes for 110 gastropods, including 40 new transcriptomes for Sacoglossa and Siphonarioidea. All 18 analyses recovered Sacoglossa as the sister group to a clade we named Pneumopulmonata, within which Siphonarioidea was sister to the remaining lineages in most analyses. Comparative modelling indicated shifts to marginal habitat (estuarine, mangrove and intertidal zones) preceded and accelerated the evolution of a pneumostome, present in the pneumopulmonate ancestor along with a one-sided plicate gill. These findings highlight key intermediate stages in the evolution of air-breathing snails, supporting the hypothesis that adaptation to marginal zones played an important role in major sea-to-land transitions.

Plasticity and artificial selection for developmental mode in a poecilogonous sea slug.

The contribution of phenotypically plastic traits to evolution depends on the degree of environmental influence on the target of selection (the phenotype) as well as the underlying genetic structure of the trait and plastic response. Likewise, maternal effects can help or hinder evolution through affects to the response to selection. The sacoglossan sea slug Alderia willowi exhibits intraspecific variation for developmental mode (= poecilogony) that is environmentally modulated with populations producing more yolk-feeding (lecithotrophic) larvae during the summer, and more planktonic-feeding (planktotrophic) larvae in the winter. I found significant family-level variation in the reaction norms between 17 maternal families of A. willowi when reared in a split-brood design in low (16 ppt) versus high (32 ppt) salinity, conditions which mimic seasonal variation in salinity of natural populations. I documented a significant response to selection for lecithotrophic larvae in high and low salinity. The slope of the reaction norm was maintained following one generation of selection for lecithotrophy. When the maternal environment was controlled in the laboratory, I found significant maternal effects, which reduced the response to selection. These results suggest there is standing genetic variation for egg-mass type in A. willowi, but the ability of selection to act on that variation may depend on the environment in which the phenotype is expressed in preceding generations.

High Rates of Self-Fertilization in a Marine Ribbon Worm (Nemertea).

Organisms capable of self-fertilization ("selfing") typically exhibit two evolutionary syndromes: uniting high inbreeding depression with low levels of selfing, or low inbreeding depression with high levels of selfing. We examined the effect of inbreeding on fecundity and time to first reproduction in an apparently self-compatible, simultaneously hermaphroditic marine nemertean worm Prosorhochmus americanus. Adult and juvenile worms were raised in isolation or in pairs. Isolated worms produced significantly more offspring than paired worms (in the adult experiment), and did not exhibit inbreeding avoidance (in the juvenile experiment). The selfing rate of six natural populations was evaluated using 17 species-specific, microsatellite markers, and was consistent with preferential selfing (mean: 0.843, SD: 0.027). Our results showed that P. americanus exhibited an interesting suite of life-history traits, uniting high colonization potential through self-fertilization and high fecundity, with no dispersive larval stage, and with moderate levels of gene flow. We believe that P. americanus is an ideal model system for studies of mating system evolution, inbreeding, and sex allocation.

Landscape structure and the genetic effects of a population collapse.

Both landscape structure and population size fluctuations influence population genetics. While independent effects of these factors on genetic patterns and processes are well studied, a key challenge is to understand their interaction, as populations are simultaneously exposed to habitat fragmentation and climatic changes that increase variability in population size. In a population network of an alpine butterfly, abundance declined 60-100% in 2003 because of low over-winter survival. Across the network, mean microsatellite genetic diversity did not change. However, patch connectivity and local severity of the collapse interacted to determine allelic richness change within populations, indicating that patch connectivity can mediate genetic response to a demographic collapse. The collapse strongly affected spatial genetic structure, leading to a breakdown of isolation-by-distance and loss of landscape genetic pattern. Our study reveals important interactions between landscape structure and temporal demographic variability on the genetic diversity and genetic differentiation of populations. Projected future changes to both landscape and climate may lead to loss of genetic variability from the studied populations, and selection acting on adaptive variation will likely occur within the context of an increasing influence of genetic drift.