Molecular Clocks in Reptiles: Life History Influences Rate of Molecular Evolution

“…included (Spearman: rS 5 0.48, P 5 0.01; Pearson: r 5 0.56, P 5 0.02). mura, and Sharp 1987; Ohta 1993; Eyre-Walker and Gaut 1997), and yet the body size effect is also a feature of total genetic distance and nonsynonymous rate (this study; Martin and Palumbi 1993; Mooers and Harvey 1994).”

“A lifehistory trend in rate of molecular evolution suggests that rates of molecular evolution must evolve over trees as life-history traits evolve, posing a dynamic picture of rate of molecular evolution, which complicates molecular phylogenetic inference (Sanderson 1997).”

“Conversely, other studies report that body size influences molecular evolution rates in reptiles and mammals (Bromham, Rambaut & Harvey, 1996; Bromham, 2002).”

“In 1993, an inverse relationship between the rate of DNA evolution and body size was observed for some genes and specie”

“Given the long generation time that characterizes turtles, our comparative analysis is consistent with the negative relationship between generation time and rate of molecular evolution found in reptiles [23] and other amniotes [24], although the observed slowdown in archosaurs and turtles may also suggest a broad, lin…”

“Selection of Phylogenetically Independent Pairs The comparative analyses in this study used phylogenetically independent sister pairs (see Felsenstein [1985]; Harvey and Pagel [1991]; Bromham et al. [1996]; and Welch and Waxman [2008]).”

“1996); and (4) body size—the smaller the body size, the higher the substitution rate (Martin and Palumbi 1993; Bromham 2002).”

“It has been hypothesised that increases in fecundity might entail an increased mutation rate [46], or reflect increased variance in offspring viability, and so lower effective population size [79].”

“…by a host of factors, ranging from generation time (e.g., Smith and Donoghue 2008), body size (e.g., Martin and Palumbi 1993; Mooers and Harvey 1994; Bromham 2002; Jackson et al. 2009), mating system (Bromham and Leys 2005), DNA repair efficiency (e.g., Drake et al. 1998; Baer et al. 2007),…”

“Among the inherited effects, body size [21-25], mass-specific metabolic rate [26], but see also [27] and generation time [28-30] have all been suggested as partial explanations of rate variation.”

“, 1998), and in each of these cases, the results are consistent with similar studies using DNA sequence data (e.g. Bromham et al., 1996; Barraclough & Savolainen, 2001; Bromham, 2002).”

“Variation in substitution rates has been linked to variation in recombination rate, efficacy of DNA repair, and life history traits such as body size or generation time (Bromham 2002; Bromham and Penny 2003; Martin and Palumbi 1993).”

“The problem we seek to address with relative rate tests is whether certain lineages or clades have evolved at different rates since their divergence from a common ancestor (e.g., as in Bromham 2002).”

“Reptilian lineages have been found to diverge from one another at significantly (perhaps eightfold) lower rates than mammalian ones (1, 4).”

“…for some vertebrate DNA sequences: species with shorter generation turnover times are assumed to have more DNA replications per unit time and will therefore accumulate more replication errors (Ohta 1993; Mooers and Harvey 1994; Bromham, Rambaut, and Harvey 1996; Li et al. 1996; Bromham 2002).”

“However, recent studies indicate that physiological and life history variables, such as generation time, metabolic rate, body size and clutch size, influence mutation rates in terrestrial vertebrates [48,49], and may affect rates of molecular evolution in reptiles as well [ 50 ].”

“Bromham, 2002; Eo and DeWoody, 2010). Macey et al. (1999) estimated a gecko-specific rate of 5.”

“This suggestion is consistent with observed associations between clutch size and rate of molecular evolution in snakes (Bromham, 2002) and between rate of molecular evolution and rate of species diversification in passerine birds and angiosperms (Barraclough et al.”

“Such violations of a molecular clock (Zuckerkandl and Pauling 1962, 1965) are ubiquitous across the tree of life and have been characterized within vertebrates (Bromham 2002; Hoegg et al. 2004; BinindaEmonds 2007), invertebrates (Hebert et al.”

“…results contradict some previous reports and theoretical expectations of an inverse relationship between BM and rates of molecular evolution in ectotherms (Bromham, 2002a; Gillooly et al., 2005), and are in line with other results confirming that the relationship between the two is not universal.”

“Background Differences in nucleotide substitution rates among taxa are a common phenomenon in molecular studies [1-7], and the presence of an exact molecular clock [8,9] appears to be a rare exception in molecular evolution, if present at all.”

“The potential correlation between ancestral small size in metazoan and fast early rates is also supported by the observation of a negative relationship between body size and rate of molecular evolution in several vertebrates clades, including birds [35], reptiles [36] and mammals [37].”

“Animal body mass, which increases in cooler terrestrial climates, has been found to inversely correlate with substitution rate ( Bromham 2002; Gillooly et al. 2005).”

“c Applies to reptile cytochrome b ( Bromham 2002, Fig. 1a).”

“…rate of the molecular clock has been shown to vary within and between species as a result of many factors including differences in metabolic rate, variation in DNA repair efficiency, mutagen exposure differences, and variation in generation time and body size (Martin & Palumbi 1993; Bromham 2002).”

“Generation time might be the most obvious factor as other researchers have found that short generation times cause faster rates of molecular evolution in taxa as different as plants (Smith & Donoghue, 2008), birds (Mooers & Harvey, 1994), primates (Sarich & Wilson, 1973), reptiles (Bromham, 2002), and 143 invertebrate…”

“This can help determine whether or not underlying shifts in molecular evolution are related to morphological rates of change and species diversity, which has been a subject of debate (Bromham et al. 2002; Davies and Savolainen 2006).”

“Similarly, there is substantial evidence for a negative correlation between body size and rates of molecular evolution in reptiles (Bromham 2002), mammals (Bromham 2011), and scombrid fishes (Qiu et al. 2014).”

“In addition, animal body mass, which is influenced by climate and increases at higher latitudes in anurans (but not urodeles) (Olalla-Tárraga & Rodríguez, 2007), has been found to inversely correlate with substitution rate (Bromham, 2002; Gillooly et al., 2005) and may therefore have contributed to our result.”

“However, body size and age at maturity have been shown to be inversely related to substitution rate (Bromham, 2002).”

“Although calibration of molecular clocks is complex (see Bromham, 2002), our data seem to be more consistent with the hypothesis proposed by Geldmacher et al. (2001).”

“Mutation rate is expected to be reflected predominantly in the silent (synonymous) substitution rate, yet the body size effect has been noted for both synonymous and nonsynonymous substitution rates (Bromham 2002) and total genetic distance (Martin and Palumbi 1993; Mooers and Harvey 1994).”

“…increase would be in contrast to the generally well-established negative correlation between body size and rate of molecular evolution (Martin & Palumbi, 1993; Mooers & Harvey, 1994; Bromham et al., 1996; Bromham, 2002; but see Slowinski & Arbogast, 1999, for critiques of some of these approaches).”

“We also note that long-lived animals with long generation times, such as crocodiles, are prone to exhibit low levels of mtDNA genetic structure [40,41,42,43], which is partially explained by their low metabolic rates [44], low mutation rates during DNA replication [45], and long longevity [46].”

“The rates of reptile mitogenome evolution vary depending on the taxonomic group and even body size of animals [73].”

“…of studies in which there is no a priori expectation of decoupled molecular and morphological evolutionary change, however, suggest that molecular and morphological evolution may at times be related (Bousquet et al. 1992; Smith et al. 1992; Savard et al. 1993; Omland 1994, 1997; Bronham 2002).”

“…operating at the level of life-history ecology and organismal biology, include generation time (Chao and Carr 1993; Martin and Palumbi 1993; Ohta 1993; Bromham 2002), homeothermy (Adachi et al. 1993), thermal habit (Bargelloni et al. 1994; Rand 1994), environmental 1176 C© 2007 The Author(s).”

“In the absence of lineage-specific substitution rates for gerrhosaurid lizards (see Bromham, 2002 ), we refrain from dating the haplotypic divergences observed among taxa.”

“and should be approached with caution (Crother & Guyer, 1996; Bromham, 2002; Graur & Martin, 2004).”

“As lineages shift their life histories in response to new ecological opportunities, this can further result in dramatic shifts in the substitution rates of entire loci (Martin and Palumbi, 1993; Bromham, 2002; Smith and Donoghue, 2008).”

“Evidence supporting the BS hypothesis comes from work across a very broad range of taxa (19, 21, 22, 28), although the effect has been disputed (29–31).”

“…evidence that rates of molecular evolution are heterogeneous among lineages, among genes, and over time (e.g., Ayala 1997; Sanderson 1997; Kumar and Hedges 1998; Thorne et al. 1998; Foote et al. 1999; Cutler 2000; Huelsenbeck et al. 2000; Sanderson and Doyle 2001; Bromham 2002; Soltis et al. 2002).”

“13(7): doi:10.1093/gbe/evab103 Advance Access publication 14 May 2021 scales, with larger species expected to have slower rates due to longer generation times (Bromham 2002; Berv and Field 2018).”

“Several empirical studies have found an inverse relationship between the tempo of microevolution and body mass (Wu & Li, 1985; Martin & Palumbi, 1993; Bromham et al., 1996; Bleiweiss, 1998a; Nunn & Stanley, 1998; Bromham, 2002; Gillooly et al., 2005; Fontanillas et al., 2007), whereas others have found no evidence of…”

“Eusociality in and of itself is already known to influence genome evolution via an effect on effective population size (Bromham and Leys 2005; Romiguier et al. 2014).”

“…time [Li et al. 1996; Bromham et al. 2002; Smith and Donoghue 2008; Thomas et al. 2010], life span [Nabholz et al. 2008; Welch et al. 2008]), body size (Bromham 2002; Wollenberg et al. 2011; Figuet et al. 2016), and environment (e.g., Davies et al. 2004; Wright et al. 2006; Lourenco et al. 2013).”

“…to 2.5 million years since divergence, placing it sometime during the end-Pliocene and Early Pleistocene (because no error terms were included in clock estimates, the ranges may be even greater and even this wide range time estimate does not have great support; Bromham 2002; Graur & Martin 2003).”

“Overall differences in evolutionary rates between lineages are widely observed (e.g., Ohta, 1993; Bromham et al., 1996; Bromham, 2002; Nabholz et al., 2008; Bromham, 2009; Welch et al., 2008; Thomas et al., 2010) and are primarily attributed to differences in generation-time, where organisms with…”

“This negative association has been identified in mammals, birds, and reptiles (Mooers and Harvey 1994; Bromham et al. 1996; Bromham 2002), and so is it in our study even after accounting for temperature.”

“The rate of the molecular clock was shown to vary within and amongst species as a result of many factors including variations in the metabolic rate, DNA repair efficiency, mutagen exposure, generation time, and body size (Martin & Palumbi, 1993; Bromham, 2002).”

“…would be difficult, if not impossible, to implement as a result of variation in coalescent times related to differences in effective population sizes and differences in lineage-specific substitution rates (Bromham, 2002; Moritz & Cicero, 2004; Hickerson, Meyer & Moritz, 2006; Pons et al ., 2006).”

“…are associated with fast life-history syndromes (e.g. small body sizes, shorter generation times) in a number of clades (Bromham et al. 1996; Bromham 2002; Qiu et al. 2014; Barrera-Redondo et al. 2018) and with high rates of cell division (Lanfear et al. 2013) (but see [Weir and Schluter…”

“lecular evolution were found in reptiles [28] and could”

“Many studies have found depressed rates of genetic evolution in larger bodied animals [7,33–39].”

“, body size), and such traits are known to impact rates of molecular evolution [32-34].”

“…analyses of molecular rates of evolution have revealed large and systematic interspecific differences (Britten 1986; Nunn and Stanley 1998; Bromham 2002; Rodriguez-Trelles et al. 2006; Nabholz et al. 2007; Smith and Donoghue 2008), which can partly be explained by variation in life…”

“Studies have found this variation in rate to be correlated to several aspects of species biology, including body size, longevity, metabolic rate, DNA repair mechanisms, and generation time (Bromham 2002; Nabholz et al. 2008; Smith and Donoghue 2008; Thomas et al. 2010).”

“However, in a broader survey of datasets, Bromham et al. (2003) found no link between rates of morphological and molecular evolution. Furthermore, Bromham et al. (2003) showed that Omland’s (1997) method may have violated the assumption”

“This mean mutation rate was based on previous studies that have estimated mutation rates for amphibians and reptiles (Bromham, 2002; Eo & DeWoody, 2010).”

“Indeed, small-bodied animals often show higher rates of substitution than large-bodied animals (reptiles: Bromham 2002; mammals: Welch et al. 2008; mammals and birds: Nabholz et al. 2013; birds: Jarvis et al. 2014; Weber et al. 2014; Berv and Field 2018).”

“Big animals and tall plants usually have relatively low rates of molecular evolution (Martin and Palumbi, 1993; Bromham, 2002; Gillooly et al., 2005; Lanfear et al., 2013; Barrera-Redondo et al., 2018).”