Comparative Genome Microsynteny Illuminates the Fast Evolution of Nuclear Mitochondrial Segments (NUMTs) in Mammals.

The escape of DNA from mitochondria into the nuclear genome (nuclear mitochondrial DNA, NUMT) is an ongoing process. Although pervasively observed in eukaryotic genomes, their evolutionary trajectories in a mammal-wide context are poorly understood. The main challenge lies in the orthology assignment of NUMTs across species due to their fast evolution and chromosomal rearrangements over the past 200 million years. To address this issue, we systematically investigated the characteristics of NUMT insertions in 45 mammalian genomes and established a novel, synteny-based method to accurately predict orthologous NUMTs and ascertain their evolution across mammals. With a series of comparative analyses across taxa, we revealed that NUMTs may originate from nonrandom regions in mtDNA, are likely found in transposon-rich and intergenic regions, and unlikely code for functional proteins. Using our synteny-based approach, we leveraged 630 pairwise comparisons of genome-wide microsynteny and predicted the NUMT orthology relationships across 36 mammals. With the phylogenetic patterns of NUMT presence-and-absence across taxa, we constructed the ancestral state of NUMTs given the mammal tree using a coalescent method. We found support on the ancestral node of Fereuungulata within Laurasiatheria, whose subordinal relationships are still controversial. This study broadens our knowledge on NUMT insertion and evolution in mammalian genomes and highlights the merit of NUMTs as alternative genetic markers in phylogenetic inference.

Swimming through the sands of the Sahara and Arabian deserts: Phylogeny of sandfish skinks (Scincidae, Scincus) reveals a recent and rapid diversification.

Large parts of the Sahara Desert and Arabia are covered by sand seas and sand dunes, which are inhabited by specialized animal communities. For example, many lizards have developed adaptations to life in loose sand, including sand-swimming behavior. The best-known sand swimmers of the Saharo-Arabia are the sandfish skinks (genus Scincus). Although there are currently only four Scincus species recognized, their phylogenetic relationships have not yet been addressed in detail. We use eight genetic markers (three mitochondrial, five nuclear) and a complete sampling of species to infer the relationships within the genus. We employ multiple phylogenetic approaches to reconstruct the evolutionary history of these skinks and to assess the level of reticulation at the onset of their radiation. Our results indicate the presence of five strongly supported species-level lineages, four represented by the currently recognized species and the fifth by S. scincus conirostris, which does not form a clade with S. scincus. Based on these results we elevate the Iranian and northern Arabian S. conirostris to the species level. The two Saharan species, S. albifasciatus and S. scincus, are sister in all analyses. Deeper relationships within the genus, however, remained largely unresolved despite the extensive genetic data set. This basal polytomy, together with the fact that we detected no sign of hybridization in the history of the genus, indicates that the diversification of the five Scincus species was rapid, burst-like, and not followed by secondary hybridization events. Divergence time estimations show a Middle Pliocene crown radiation of the genus (3.3 Mya). We hypothesize that the aridification of the Saharo-Arabia that began in the Late Miocene triggered the initial diversification of Scincus, and that the subsequent expansion of sand deserts enabled their dispersal over the large Saharan and Arabian range. We discuss the evolution of body form in sand swimming lizards and ponder how Scincus retained their fully limbed morphology despite being sand swimmers that are typically limbless.

Ancient diversification, biogeography, and the role of climatic niche evolution in the Old World cat snakes (Colubridae, Telescopus).

The process of species diversification is often associated with niche shifts in the newly arising lineages so that interspecific competition is minimized. However, an opposing force known as niche conservatism causes that related species tend to resemble each other in their niche requirements. Due to the inherent multidimensionality of niche space, some niche components may be subject to divergent evolution while others remain conserved in the process of speciation. One such possible component is the species' climatic niche. Here, we test the role of climatic niche evolution on the diversification of the Old World cat snakes of the genus Telescopus. These slender, nocturnal snakes are distributed in arid and semiarid areas throughout Africa, southwest Asia and adjoining parts of Europe. Because phylogenetic relationships among the Telescopus species are virtually unknown, we generated sequence data for eight genetic markers from ten of the 14 described species and reconstructed a time-calibrated phylogeny of the genus. Phylogenetic analysesindicate that the genus is of considerably old origin that dates back to the Eocene/Oligocene boundary. Biogeographical analyses place the ancestor of the genus in Africa, where it diversified into the species observed today and from where it colonized Arabia and the Levant twice independently. The colonization of Arabia occurred in the Miocene, that of the Levant either in the Late Oligocene or Early Miocene. We then identified temperature and precipitation niche space and breadth of the species included in the phylogeny and examined whether there is phylogenetic signal in these climatic niche characteristics. Despite the vast range of the genus and its complex biogeographic history, most Telescopus species have similar environmental requirements with preference for arid to semiarid conditions. One may thus expect that the genus' climatic niche will be conserved. However, our results suggest that most of the climatic niche axes examined show no phylogenetic signal, being indicative of no evolutionary constraints on the climatic niche position and niche breadth in Telescopus. The only two variables with positive phylogenetic signal (temperature niche position and precipitation niche breadth) evolved under the Brownian motion model, also indicating no directional selection on these traits. As a result, climatic niche evolution does not seem to be the major driver for the diversification in Telescopus.

Duplications of Human Longevity-Associated Genes Across Placental Mammals.

Natural selection has shaped a wide range of lifespans across mammals, with a few long-lived species showing negligible signs of ageing. Approaches used to elucidate the genetic mechanisms underlying mammalian longevity usually involve phylogenetic selection tests on candidate genes, detections of convergent amino acid changes in long-lived lineages, analyses of differential gene expression between age cohorts or species, and measurements of age-related epigenetic changes. However, the link between gene duplication and evolution of mammalian longevity has not been widely investigated. Here, we explored the association between gene duplication and mammalian lifespan by analyzing 287 human longevity-associated genes across 37 placental mammals. We estimated that the expansion rate of these genes is eight times higher than their contraction rate across these 37 species. Using phylogenetic approaches, we identified 43 genes whose duplication levels are significantly correlated with longevity quotients (False Discovery Rate (FDR) < 0.05). In particular, the strong correlation observed for four genes (CREBBP, PIK3R1, HELLS, FOXM1) appears to be driven mainly by their high duplication levels in two ageing extremists, the naked mole rat (Heterocephalus glaber) and the greater mouse-eared bat (Myotis myotis). Further sequence and expression analyses suggest that the gene PIK3R1 may have undergone a convergent duplication event, whereby the similar region of its coding sequence was independently duplicated multiple times in both of these long-lived species. Collectively, this study identified several candidate genes whose duplications may underlie the extreme longevity in mammals, and highlighted the potential role of gene duplication in the evolution of mammalian long lifespans.