Metabolic Rate, Generation Time, and the Rate of Molecular Evolution in Birds

“Genetic distances of species pairs, measured relative to an outgroup, by either the relative rates test or DNA hybridisation distances, should thus be greater in species occupying high-energy areas (Li & Graur, 1991; Mooers & Harvey, 1994; Bromham & Cardillo, 2003).”

“This is consistent with the observations that ECTOTHERMS have lower substitution rates than ENDOTHERMS 36, that smaller-bodied species of vertebrates with faster metabolic rates have higher substitution rates than larger-bodied specie”

“The generation time hypothesis (Li et al. 1987; Ohta 1993; Mooers and Harvey 1994; Bromham et al. 1996) expresses that species with a shorter generation time experience a higher number of DNA replication rounds per year and thus a higher number of replication errors per time unit.”

“In addition, direct tests for associations between RMR and the rates of mutation or molecular evolution have usually produced nonsignificant results (Mooers & Harvey, 1994; Bromham, Rambaut & Harvey, 1996; Gissi et al., 2000; Lanfear et al., 2007; McGaughran & Holland, 2010; Feng et al., 2014).”

“Uniform rates of change across a tree cannot be assumed, as lineage-specific rate variation has been demonstrated for many taxonomic groups (e.g., mammals [Bromham, Rambaut, and Harvey 1996], birds [Mooers and Harvey 1994], and plants [Bosquet et al. 1992; Gaut et al. 1992]).”

“Using DNA-DNA hybridization data (and a smaller dataset), Mooers and Harvey [32] found no support for the metabolic rate hypothesis, but reported a significant generation time effect.”

“The inverse relationship between rate of molecular evolution and body size has been described for a range of vertebrate taxa, including mammals, birds, reptiles, amphibians, and fishes (Bromham, 2002; Bromham et al., 1996; Martin and Palumbi, 1993; Mooers and Harvey, 1994).”

“Tanimura 1987; Ohta 1993; Mooers and Harvey 1994; Bromham, Rambaut, and Harvey 1996; Bromham”

“However, neither of these propositions appears to have survived direct scrutiny (Mooers and Harvey 1994; Van Den Bussche et al. 1998).”

“Comparative studies have identified species characteristics that are correlated with variation in rate of evolution, such as body size, generation time, metabolic rate and fecundity [56,57, 59 ].”

“There is also increasing evidence, particularly in vertebrates, that some of this lineage-specific rate variation may be predictable from aspects of a species' biology [8-17].”

“…generation time does not appear to a¡ect speed of selection (Rosenheim & Tabashnik 1993; Mooers & Harvey 1994; Bromham et al. 1996), although it has been linked to the rate of neutral molecular evolution (Sibley & Ahlquist 1990; Martin & Palumbi 1993; Mooers & Harvey 1994; Bromham et al. 1996).”

“However, studies that have examinedmultiple life-history variables have found no significant association between metabolic rate and rate of molecular evolution beyond its covariance with other lifehistory variables, such as body size, generation time, and longevity in birds (47, 71) and other animals (50, 71, 72).”

“…original explanation for this rate heterogeneity is that species with shorter generation times have a greater number of DNA replications per year, thus incurring an increased chance of replication error per unit time (Li, Tanimura, and Sharp 1987; Ohta 1993; Mooers and Harvey 1994; Li et al. 1996).”

“The variation in mutation rate among different lineages may also be due to variation of metabolic rate or of life history (Martin and Palumbi, 1993; Moers and Harvey, 1994; Martin, 1999; Bromham, 2002) and to varition of DNA repair efficiency (Britten, 1986).”

“, 2004), generation time (Martin and Palumbi, 1993; Mooers and Harvey, 1994), DNA replication accuracy (Hebert et al.”

“…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).”

“…are influenced 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;…”

“Other factors might influence the rates of both morphological and molecular evolution—for example, body size, generation time, or selective sweeps (see, e.g., Mooers and Harvey 1994; Bromham et al. 1996; Omland 1997).”

“There have been several studies that show a relationship between the rate of molecular evolution and physiological properties of the organisms like generation time, metabolic rate, and body size (Li 1993; Martin and Palumbi 1993; Mooers and Harvey 1994; Gillooly et al. 2005).”

“However, although birds show a generation time effect, demonstrated for DNA hybridization data ( Mooers & Harvey, 1994 ), and there is evidence that average body size for bird species decreases towards the equator (Blackburn & Gaston, 1996; Cardillo, 2002), we did not find any association between molecular rates and l…”

“Evidence on the association between generation time and the rate of molecular evolution has been also found in birds (Mooers and Harvey 1994), but not in insects (Crozier and Crozier 1992).”

“…taxa—e.g., geese (Shields and Wilson, 1987) and Hawai’ian honey-creepers (Tarr and Fleischer, 1993)—but there is some evidence of lineage-speci W c rate variation in birds (see Lovette, 2004), e.g., due to generation time (Mooers and Harvey, 1994) and population size (Johnson and Seger, 2001).”

“, 1992), the effect of generation time on rates of avian molecular evolution (Mooers and Harvey, 1994) the evolution of avian mating systems and the association between mating systems and pair-bond length (Temrin and Sillen-Tullberg, 1994).”

“However, plants do not have a segregated germ line, and thus should show no correlation between the number of generations and the number of potentially mutation-inducing replications in the history of their gametes, which is the explanation typically proffered for the “generation time hypothesis” (Mooers and Harvey 19…”

“The body size trend in molecular evolution rate in vertebrates (Martin and Palumbi, 1993; Mooers and Harvey, 1994; Bromham et al., 1996) has prompted the suggestion that the presumed small body size of stem lineages of major radiations could generate fast early rates (e.”

“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].”

“However, the evidence that species life histories are linked with the rate of molecular evolution is mixed (Mooers & Harvey 1994; Smith & Donoghue 2008; Lanfear et al. 2010a; Thomas et al. 2010; Thomson et al. 2014).”

“…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 species (Thomas et al., 2010).”

“While molecular clock has been largely accepted as a null hypothesis of molecular evolution, many possible influencing factors have been proposed and investigated either in animals or in plants during these decades, including changes in population size, protein dispensability, efficiency of DNA replication and repair…”

“The body size trend in molecular evolution rate in tetrapod vertebrates (Martin & Palumbi 1993; Mooers & Harvey 1994; Bromham et al. 1996) has prompted the suggestion that the presumed small size of the earliest metazoans generated faster rates early in the metazoan radiation (Conway Morris 1998).”

“…and heterogeneous preservation rates among clades, among environments, and over geological time (e.g., Bosquet et al. 1992; Gaut et al. 1992; Mooers and Harvey 1994; Mooers 1995; Bromham et al. 1996; Huelsenbeck and Kirkpatrick 1996; Mooers and Heard 1997; Ayala et al. 1998; Rambaut and…”

“definition that is used for T; for example, age at first reproduction has been interpreted as T in several studies [1,7–10].”

“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).”

“…proportions of sites under selection in each locus (Kimura and Ohta 1974, Mouchiroud et al. 1995), b) by disparities in species longevity, generation time, metabolic rate, and body size (i.e. lineage effects; Martin and Palumbi 1993, Mooers and Harvey 1994, Nabholz et al. © 2015 The Authors.”

“, [2–6]).”

“Variation in rates of sequence substitution is unpredictable and often rather large; furthermore, different lineages may have different patterns of rate variation [4-6,8,9].”

“Shorter generation times have been associated with faster molecular evolution in birds (Mooers and Harvey 1994), mammals (Bromham et al. 1996, Welch et al. 2008) and invertebrates (Thomas et al. 2010).”

“Given these considerations and the close relationship between metabolism and body mass, the latter may be a more accurate predictor of the effect of metabolic rate on genomic evolution than are currently available experimental values of basal metabolic rate (Mooers and Harvey 1994).”

“Body size is correlated with generation time (Martin & Palumbi 1993, Mooers & Harvey 1994, Smith & Donoghue 2008, April et al. 2013) and population size (Damuth 1981, Marquet et al. 1995), 2 factors that tightly inter- act with mutations to drive genetic drift (Kimura 1983) and result in varying…”

“Of the work that has addressed the alternatives, Mooers and Harvey (32) found that age at first birth in birds was significantly related to the rate of molecular evolution in DNA–DNA hybridization data, but BS was not.”

“Results were converted into biologically informative values assuming an average mutation rate of 4.6 × 10−9 mutations per site per generation (Smeds et al., 2016) and a generation time of 1 year (Mooers & Harvey, 1994).”

“…(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 such a relationship (Mooers & Harvey, 1994; Spradling et al., 2001; Thomas et al., 2006).”

“However, neither of these propositions appears to have survived direct scrutiny (Mooers and Harvey 1994; Van Den Bussche et al. 1998).”

“However, there is more inconsistency in the correlation between metabolic rate and sequence evolution than for the above life history traits; therefore, its effects are likely not as universal or strong (Mooers and Harvey 1994; Bromham et al. 1996; Rowe and Honeycutt 2002; Gillooly et al. 2005) (table 1).”

“Another explanation that has been proposed is the generation time effect based on the assumption that germ-lines of species with shorter generation times have a greater number of DNA replications per year, and thus a greater chance of replication errors per unit time (Li, Tanimura & Sharp, 1987; Ohta, 1993; Mooers & H…”

“generation times and evolutionary rates [52, 53].”