Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards

Abstract

Climatic conditions changing over time and space shape the evolution of organisms at multiple levels, including temperate lizards in the family Lacertidae. Here we reconstruct a dated phylogenetic tree of 262 lacertid species based on a supermatrix relying on novel phylogenomic datasets and fossil calibrations. Diversification of lacertids was accompanied by an increasing disparity among occupied bioclimatic niches, especially in the last 10 Ma, during a period of progressive global cooling. Temperate species also underwent a genome-wide slowdown in molecular substitution rates compared to tropical and desert-adapted lacertids. Evaporative water loss and preferred temperature are correlated with bioclimatic parameters, indicating physiological adaptations to climate. Tropical, but also some populations of cool-adapted species experience maximum temperatures close to their preferred temperatures. We hypothesize these species-specific physiological preferences may constitute a handicap to prevail under rapid global warming, and contribute to explaining local lizard extinctions in cool and humid climates.

Chromosome Painting Does Not Support a Sex Chromosome Turnover in Lacerta agilis Linnaeus, 1758

“…Meanwhile, resolving this contradiction is crucial for understanding the Lisachov et al Cytogenet Genome Res 2020;160:134-140 DOI: 10.1159/000506321 136 patterns of evolution of sex-determining mechanisms in reptiles in general. If confirmed, "the curious case of Lacerta agili s" could become an interesting model to study the processes of sex determination evolution, since the sex chromosomes of this species might represent a young sex chromosome system with a known time of origin, based on the established phylogenetic tree of Lacertidae [Garcia-Porta et al, 2019], and with an autosomal homologue in the genomes of closely related species [Andrade et al, 2019].…”

Flight demand and environmental niche are associated with molecular evolutionary rates in a large avian radiation

“…The impact of environmental temperature and UV radiation on mutation rates is also likely to be negligible in species that regulate their internal energy levels and whose gametes do not undergo direct exposure to environmental factors, such as most endotherms (but see Gillman et al 2009). This contrasts with the impact that temperature can have on the mutation rates in organisms that are more exposed to environmental conditions, such as many marine taxa (Allen et al 2006; Wright et al 2010b), plants (Davies et al 2004; Wright et al 2006; Gillman et al 2010), amphibians (Wright et al 2010a), and reptiles (Garcia-Porta et al 2019).…”

“…The factors driving molecular evolution are a long standing matter of interest in the biological sciences. Some of the most studied factors correlating with rates of molecular evolution on a macroevolutionary scale include life-history traits (Bromham 2011), metabolic activity (e.g., Garcia-Porta et al 2019) and environmental energy (Wright et al 2006). These factors are also likely to interact, with the evolutionary outcome depending on the balance between the costs of sources of deleterious mutations and the requirements of the particular lifestyle of species (Bromham 2009).…”

“…Mass-specific metabolic rate is inversely associated with body mass (Martin & Palumbi 1993), which provides one explanation for the accelerated rates of molecular evolution in small vertebrates compared to large ones. While there is some evidence that metabolic rates are indeed associated with rates of molecular evolution (Bleiweiss 1998; Gillooly et al 2005, 2007; Garcia-Porta et al 2019), multiple studies have not found such an association (Mooers & Harvey 1994; Bromham et al 1996; Lanfear et al 2007; Galtier et al 2009; Rolland et al 2016).…”

“…Another widely studied factor that might drive molecular evolutionary rate is environmental energy through its mutagenic effect on the genome (Martin & Palumbi 1993; Allen et al 2006). Studies in organisms including plants (Davies et al 2004; Wright et al 2006), marine organisms (Wright et al 2010b), and lizards (Garcia-Porta et al 2019) have all found associations between environmental energy and molecular rates. The link between energy and molecular evolution is often inferred using environmental temperature as a proxy of available energy (Wright et al 2006).…”