Evolution of horn length and lifting strength in the Japanese rhinoceros beetle Trypoxylus dichotomus.

What limits the size of nature's most extreme structures? For weapons like beetle horns, one possibility is a tradeoff associated with mechanical levers: as the output arm of the lever system-the beetle horn-gets longer, it also gets weaker. This "paradox of the weakening combatant" could offset reproductive advantages of additional increases in weapon size. However, in contemporary populations of most heavily weaponed species, males with the longest weapons also tend to be the strongest, presumably because selection drove the evolution of compensatory changes to these lever systems that ameliorated the force reductions of increased weapon size. Therefore, we test for biomechanical limits by reconstructing the stages of weapon evolution, exploring whether initial increases in weapon length first led to reductions in weapon force generation that were later ameliorated through the evolution of mechanisms of mechanical compensation. We describe phylogeographic relationships among populations of a rhinoceros beetle and show that the "pitchfork" shaped head horn likely increased in length independently in the northern and southern radiations of beetles. Both increases in horn length were associated with dramatic reductions to horn lifting strength-compelling evidence for the paradox of the weakening combatant-and these initial reductions to horn strength were later ameliorated in some populations through reductions to horn length or through increases in head height (the input arm for the horn lever system). Our results reveal an exciting geographic mosaic of weapon size, weapon force, and mechanical compensation, shedding light on larger questions pertaining to the evolution of extreme structures.

Genomic patterns of divergence in the early and late steps of speciation of the deep-sea vent thermophilic worms of the genus Alvinella.

BACKGROUND: The transient and fragmented nature of the deep-sea hydrothermal environment made of ridge subduction, plate collision and the emergence of new rifts is currently acting to separate of vent populations, promoting local adaptation and contributing to bursts of speciation and species specialization. The tube-dwelling worms Alvinella pompejana called the Pompeii worm and its sister species A. caudata live syntopically on the hottest part of deep-sea hydrothermal chimneys along the East Pacific Rise. They are exposed to extreme thermal and chemical gradients, which vary greatly in space and time, and thus represent ideal candidates for understanding the evolutionary mechanisms at play in the vent fauna evolution. RESULTS: We explored genomic patterns of divergence in the early and late stages of speciation of these emblematic worms using transcriptome assemblies and the first draft genome to better understand the relative role of geographic isolation and habitat preference in their genome evolution. Analyses were conducted on allopatric populations of Alvinella pompejana (early stage of separation) and between A. pompejana and its syntopic species Alvinella caudata (late stage of speciation). We first identified divergent genomic regions and targets of selection as well as their position in the genome over collections of orthologous genes and, then, described the speciation dynamics by documenting the annotation of the most divergent and/or positively selected genes involved in the isolation process. Gene mapping clearly indicated that divergent genes associated with the early stage of speciation, although accounting for nearly 30% of genes, are highly scattered in the genome without any island of divergence and not involved in gamete recognition or mito-nuclear incompatibilities. By contrast, genomes of A. pompejana and A. caudata are clearly separated with nearly all genes (96%) exhibiting high divergence. This congealing effect however seems to be linked to habitat specialization and still allows positive selection on genes involved in gamete recognition, as a possible long-duration process of species reinforcement. CONCLUSION: Our analyses highlight the non-negligible role of natural selection on both the early and late stages of speciation in the iconic thermophilic worms living on the walls of deep-sea hydrothermal chimneys. They shed light on the evolution of gene divergence during the process of speciation and species specialization over a very long period of time.

Comparative genomic and transcriptomic analyses of transposable elements in polychaetous annelids highlight LTR retrotransposon diversity and evolution.

BACKGROUND: With the expansion of high throughput sequencing, we now have access to a larger number of genome-wide studies analyzing the Transposable elements (TEs) composition in a wide variety of organisms. However, genomic analyses often remain too limited in number and diversity of species investigated to study in depth the dynamics and evolutionary success of the different types of TEs among metazoans. Therefore, we chose to investigate the use of transcriptomes to describe the diversity of TEs in phylogenetically related species by conducting the first comparative analysis of TEs in two groups of polychaetes and evaluate the diversity of TEs that might impact genomic evolution as a result of their mobility. RESULTS: We present a detailed analysis of TEs distribution in transcriptomes extracted from 15 polychaetes depending on the number of reads used during assembly, and also compare these results with additional TE scans on associated low-coverage genomes. We then characterized the clades defined by 1021 LTR-retrotransposon families identified in 26 species. Clade richness was highly dependent on the considered superfamily. Copia elements appear rare and are equally distributed in only three clades, GalEa, Hydra and CoMol. Among the eight BEL/Pao clades identified in annelids, two small clades within the Sailor lineage are new for science. We characterized 17 Gypsy clades of which only 4 are new; the C-clade largely dominates with a quarter of the families. Finally, all species also expressed for the majority two distinct transcripts encoding PIWI proteins, known to be involved in control of TEs mobilities. CONCLUSIONS: This study shows that the use of transcriptomes assembled from 40 million reads was sufficient to access to the diversity and proportion of the transposable elements compared to those obtained by low coverage sequencing. Among LTR-retrotransposons Gypsy elements were unequivocally dominant but results suggest that the number of Gypsy clades, although high, may be more limited than previously thought in metazoans. For BEL/Pao elements, the organization of clades within the Sailor lineage appears more difficult to establish clearly. The Copia elements remain rare and result from the evolutionary consistent success of the same three clades.

Mollusc genomes reveal variability in patterns of LTR-retrotransposons dynamics.

BACKGROUND: The three superfamilies of Long Terminal Repeat (LTR) retrotransposons are a widespread kind of transposable element and a major factor in eukaryotic genome evolution. In metazoans, recent studies suggested that Copia LTR-retrotransposons display specific dynamic compared to the more abundant and diverse Gypsy elements. Indeed, Copia elements show a relative scarcity and the prevalence of only a few clades in specific hosts. Thus, BEL/Pao seems to be the second most abundant superfamily. However, the generality of these assumptions remains to be assessed. Therefore, we carried out the first large-scale comparative genomic analysis of LTR-retrotransposons in molluscs. The aim of this study was to analyse the diversity, copy numbers, genomic proportions and distribution of LTR-retrotransposons in a large host phylum. RESULTS: We compare nine genomes of molluscs and further added LTR-retrotransposons sequences detected in databases for 47 additional species. We identified 1709 families, which enabled us to define 31 clades. We show that clade richness was highly dependent on the considered superfamily. We found only three Copia clades, including GalEa and Hydra which appear to be widely distributed and highly dominant as they account for 96% of the characterised Copia elements. Among the seven BEL/Pao clades identified, Sparrow and Surcouf are characterised for the first time. We find no BEL or Pao elements, but the rare clades Dan and Flow are present in molluscs. Finally, we characterised 21 Gypsy clades, only five of which had been previously described, the C-clade being the most abundant one. Even if they are found in the same number of host species, Copia elements are clearly less abundant than BEL/Pao elements in copy number or genomic proportions, while Gypsy elements are always the most abundant ones whatever the parameter considered. CONCLUSIONS: Our analysis confirms the contrasting dynamics of Copia and Gypsy elements in metazoans and indicates that BEL/Pao represents the second most abundant superfamily, probably reflecting an intermediate dynamic. Altogether, the data obtained in several taxa highly suggest that these patterns can be generalised for most metazoans. Finally, we highlight the importance of using database information in complement of genome analyses when analyzing transposable element diversity.