Convergent evolution to subterranean life in Aselloidea

Aselloidea are cool crustaceans that like to go underground.

Subterranean animals display a set of convergent traits described as the troglomorphic syndrome. This includes morphological (e.g. eyes or pigmentation reduction/vanishing and hypertrophy of non ocular sensory organs), physiological (e.g. hypometabolism, resistance to starvation and hypoxia), behavioral convergences (e.g. aggressiveness reduction, loss of pre-copulatory amplexus, loss of circadian rhythm) but also convergences in life history traits (e.g. high longevity, low fecundity). This syndrome is one of the most blatant examples of massive (across thousands of species) and widespread (across all metazoan) phenotypic convergences. While subterranean organisms are iconic and widespread examples of convergence, most subterranean species do not have closely related surface species, making comparative analyses difficult.

The Asellidae is a rare exception to this rule. Asellidae is one of the largest Isopods (Pancrustacean) family with ca. 333 described species. Most Asellidea subterranean species (ca. 80%) colonized groundwater independently and convergently developed the troglomorphic syndrome. Surface species are also found in most Asellidae clades, easing comparative analyses as a reference species with valuable information on the ancestral state is always close at hand. During this project we will particularly study the convergent gain of increased longevity and convergent loss of the eye and pigmentation using 15 independent pairs of surface and subterranean Aselloidea.

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Convergent evolution to saltwater in Gerromorpha

Gerromorpha are cool insects that like it wet.

The semi-aquatic bugs (Heteroptera, Gerromorpha) have conquered water surfaces worldwide including the oceans, and represent by far the dominating group of insects in these habitats. Out of the million or so described species of insects, the Gerromorpha which initially specialize in fresh water zones, have been astonishingly successful in colonizing marine habitats, including the open ocean. Ancestral character reconstruction revealed that out of the 18 known marine lineages, 14 transitions were completed independently from each other in the group. The other 140 genera remain in fresh water zones. The marine versus freshwater preference covers both micro- and macro-evolutionary scales. In some genera, both marine and freshwater populations of the same species can be found, but some lineages either at the family level or at the genus level are exclusively marine.

The primary environmental change associated with the transition of freshwater populations to marine habitats is increased salinity, which affects stasis of body fluids and increases surface tension. We expect that each time a lineage occupies marine environment, changes in the building of the hydrophobic bristles covering the legs, that exploit surface tension, as well as physiological changes to cope with high salt content should ensue. Therefore, to study convergence of the semi-aquatic bugs to marine environments, we chose to focus on these two central traits.

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Convergent evolution to arid environments in rodents

Rodents are cute, and some like it hot.

Rodentia is the largest group of mammals with more than 2200 species representing circa 42 % of mammalian biodiversity, and include the most heavily studied mammal species (the mouse). Since their origin 60-70 million years ago, they colonized all the continents to the exception of the Antarctica. They inhabit almost all types of environments and present an important ecological and morphological diversity, which makes them perfect to study convergence in mammals.

Adaptation to arid environments occurred several times independently during rodent history in various groups and different places of the world, the most extreme case being adaptation to life in deserts (e.g. gerbils in Africa or the kangaroo rats in the Americas). Rodents inhabiting these environments present a whole range of morphological, physiological and behavioral adaptations in order to cope with limited water and food availability. Some of these adaptations involve the nervous system (e.g. anti-diuretic hormone regulation), but adaptation of kidney physiology is key. For example, it is known that many species have increased urine concentrating capacities, notably the gerbil, spiny mouse, kangaroo rat and syrian hamster, all included in this project) which is associated to an increase of the kidney medulla size. On top of that, kidney development has been heavily studied in mouse and spatial expression in the mature kidney is described at the cellular level. In conclusion, adaptation to arid environments involves a number of different traits justifying to study convergence in CDS, and expression in kidney is highly relevant to study convergence in expression levels. Our dataset will comprise 7 pairs representing 7 independent transitions to arid environments, occurring between 10 and 65 million years ago (i.e. the roots of rodent phylogeny).

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Sampling and data acquisition

Large-scale generation of RNA-seq data.

In each of the three groups of organisms, species with contrasted phenotypes have been sampled. These existing samples will be complemented in the early phases of the project. For each individual, RNA-seq data will be generated. Then a robust pipeline will be applied to the data to assemble transcript sequences, annotate gene families, generate gene phylogenies and compute expression levels. The same pipeline will be applied to all data sets so as to make comparison across species and across groups of animals natural.

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Analysis of sequence evolution

Finding sequence changes correlated with phenotypic changes.

Genomes undergo sequence changes all the time. Some of those changes have phenotypic consequences, while others have very little effect. We will develop statistical methods to identify sequence changes that are most likely to be associated with the convergent phenotypic changes of interest. We plan on analysing gene duplications and losses, sequence substitutions, and insertion-deletions. We will use probabilistic models of sequence evolution and will account for the effects of incomplete lineage sorting.

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Analysis of gene expression evolution

Comparing gene expression across species.

We will generate expression data in species with convergent and ancestral phenotypes. We will analyse this expression data using models derived from Brownian motion (e.g. Ornstein-Uhlenbeck models). Current state-of-the art methods allow jointly considering intra- and inter-species data, and we plan on building upon such methods to identify genes whose expression underwent changes correlated to the convergent phenotypes of interest.

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