EVOLUTIONARY QUANTITATIVE GENETICS: HOW LITTLE DO WE KNOW?

“…fitness to our model, a pattern of genotypic variation that is “ a general feature ” of continuously varying traits such as fitness in natural systems (Barton & Turelli, 1989, p. 345, see also Des Marais et al., 2013; Gupta & Lewontin, 1982; Haldane, 1946; Sultan, 2015 and references therein;…”

“36 A key challenge in evolutionary biology is to understand the mechanisms maintaining genetic 37 diversity in natural populations (Barton & Turelli 1989; Brooks 2002; Endler 1986; Futuyma 38 2005; Hartl & Clark 1997; Hedrick 1986; Hedrick 2006; Kotiaho, Simmons & Tomkins 2001; 39 Lewontin 1974;…”

“Understanding how this type of variation persists 391 despite strong directional selection is a major challenge (Barton & Turelli 1989).”

“In some models divergence is facilitated by few ‘speciation genes’ while in others the associations built up across many selected loci contribute to the process of speciation (Barton & Turelli, 1989).”

“Assuming certain transmission rules and fitness differences, quantitative genetic models predict how the frequency distribution changes under mutation, selection, drift, and recombination (Lynch and Walsh [22], Barton and Turelli [4]).”

“While most quantitative traits, including human diseases, show substantial heritability in most populations, their allelic architecture remains poorly understood [88,89].”

“One unresolved issue is whether genetic variation for ®tness and ®tness components is caused by many polygenes of small e ect, or whether genes of major e ect can segregate despite natural selection (Barton & Turelli, 1989; Orr & Coyne, 1992).”

“The underlying genetics of phenotypes plays an important role in their evolutionary dynamics (Barton and Turelli, 1989) and in several evolutionary controversies, such as the basis for the maintcnance of genetic variation (Turelli, 1988).”

“environmental variation might maintain genetic variance (Barton and Turelli 1989; Johnson and Barton 2005): do”

“Hence, the evolutionary statistics of molecular quantitative traits have to go beyond traditional quantitative genetics [2–11].”

“The genetic variation is controlled by a number of genes, quantitative trait loci (QTL), which together determine the phenotype, even though each gene, by itself, may contribute only a small fraction of the observed trait value (Barton and Turelli 1989; Tanksley 1993).”

“This opinion was confirmed by studies in quantitative genetics in which normal distributions of characters are observed independently of the frequency distribution of specific alleles (Barton and Turelli, 1989).”

“the consequence of greater additive genetic variation leading to large environmental variances (Barton and Turelli 1989; Roff 1997).”

“Trade-offs resulting from pleiotropy may constrain evolutionary change within both field and laboratory environments (Barton and Turelli 1989; Partridge and Sibly 1991; Hoffmann et al. 1995).”

“Theoretical predictions on the maintenance of variation, the evolution of sex and recombination, and the genetic load all depend on mutational parameters (Kondrashov, 1988, 1995; Barton & Turelli, 1989; Charlesworth, 1990; Crow, 1993; Charlesworth & Hughes, 1998).”

“Quantitative genetic theory focuses on finding the underlying genetic variation in genes by applying the classical infinitesimal (polygenic) model [2, 6].”

“Theoretical models (Lande 1979; Turelli 1988; Barton and Turelli 1989) and empirical studies (Arnold 1981; Lofsvold 1986; Cheverud 1988; Kohn and Atchley 1988; Wilkinson et al. 1990; Shaw et al. 1995; Roff 1996; Bégin and Roff 2003) do not agree in their assessment of the degree of structural…”

“However, it is unclear how the maintenance of this standing variation might be affected by environmental fluctuations, although it has been suggested that the propensity to maintain variation may be higher in more rapidly fluctuating environments (Barton and Turelli 1989).”

“The magnitude of per-generational increase in genetic variance due to spontaneous mutations (VM) is important for a wide range of genetic and evolutionary phenomena, including the maintenance of quantitative genetic variance (Lynch 1988; Barton and Turelli 1989; Johnson and Barton 2005).”

“The genetic basis of the traits will also determine the extent to which selection may alter G [21]; for traits affected by many loci and alleles per locus, with a multivariate normal distribution of effects, changes in allele frequencies in response to selection are likely to be slow [22], which may facilitate genetic…”

“While existing models accommodate variation in traits under both stabilizing and directional selection ( Barton & Turelli, 1989; Kondrashov & Houle, 1994; Fry, Heinsohn & Mackay, 1998a; Barton & Keightley, 2002), we expect different genetic architecture to result from stabilizing rather than directional selection (Cha…”

“Additive genetic variance, development, and evolution The relationship between additive genetic variance and longterm evolutionary change has been an important question for evolutionary biologists (Barton & Turelli 1989).”

“The issue is of some gen­ eral interest since the reasons why heritable variation persists in nature re­ main obscure (e.g. Barton and Turelli 1989 ).”

“Such a roadmap has been developed by several workers including Bulmer (1972), Barton and Turelli (1989), and Bürger (2000).”

“Our results underscore the challenges in predicting morphological and life-history trait changes resulting from outbreeding because of temporally changing correlations between single traits (such as size-at-age with growth rate) or because the expression of single ‘traits’ can result from combinations of other traits…”

“Extensions of phenotypic evolutionary models with diploid and sexual inheritance often assume partially dominant inheritance (e.g., Matessi and Di Pasquale 1996; Geritz et al. 1998; Kisdi and Geritz 1999), possibly because assuming small mutational effects implies approximately additive genetics in mutant heterozygote…”

“The genetic underpinnings of fitness have been subject to intense theoretical scrutiny in a wide variety of areas of evolutionary biology and animal breeding (Kruuk et al. 2008; Roff 2007; Merilä and Sheldon 1999, 2000; Barton and Turelli 1989; Fisher 1930).”

“Environmental variation has been considered a potential contributor (Barton and Turelli, 1989; Gillespie, 1991), although the temporal extent considered was small.”

“PREDICTIONS of the evolutionary dynamics of quan-titative traits are highly sensitive to the genetic architecture assumed to underlie them (Barton and Turelli 1989).”

“This is in line with evolutionary theory that antagonistic pleiotropy preserves genetic variation, as in Rose's (1982) model of ‘antagonistic pleiotropy’ between fitness components, and also discussed by Barton and Turelli (1989), or shown experimentally in biological models (Pemberton et al.”

“How high levels of genetic variation are maintained in quantitative traits under stabilizing selection remains a major problem in evolutionary biology (Barton & Turelli, 1989; Johnson & Barton, 2005).”

“A variety of mechanisms can allow for the maintenance of multiple genetic colour morphs at appreciable levels within populations (Barton & Turelli, 1989), including negative frequency dependence (Maynard Smith, 1982; Parker, 1984; Gray & McKinnon, 2007), spatially variable selection (i.e.…”

“But phenotypic selection gradient theory is controversial (Turelli 1984; Barton and Turelli 1989) precisely because it must be harnessed to a genetic theory in order to have evolutionary implications.”

“Combining small effect variants of opposite sign may result in a sum of close to zero (Barton and Turelli 1989; Griswold and Whitlock 2003), resulting in an apparently smaller contribution of trans variance.”

“If gene complexes encompassing genes of large nonadditive effects are an important feature of the genetic architecture not only of recently evolved domesticated but also natural plant species, then the practice of ignoring such major genetic coadaptation in quantitative genetic models of speciation (e.g., Barton and T…”

“Current evolutionary thought, however, assumes that most adaptive trait variation results from large numbers of additive gene loci, each with infinitesimal small effects (Falconer, 1981; Barton and Turelli, 1989), although this paradigm has been challenged in the last decade (Orr and Coyne, 1992).”

“What does that say about the status of genic selectionism as a serious scientific research program? 10 See Barton and Turelli (1989), and Turelli and Barton (1990).”

“The paradox of widespread segregating variation for quantitative traits in natural populations, despite strong stabilizing and directional selection that should eliminate variation, is unresolved (Barton & Turelli, 1989).”

“This high heritability found for most analyzed traits may be explained by a large genetic variance rather than by a smaller environmental variance, as already was suggested by Barton and Turelli (1989) [54] and by Badri et al. (2016) [55].”

“The following five processes are generally thought ( Barton & Turelli, 1989; Maynard Smith, 1998) to encompass the most likely candidates maintaining genetic variation in morphological traits: (1) frequencydependent selection, (2) temporal environmental heterogeneity and genotype by environment interaction, (3) spatia…”

“Although evidence of phenotypic variation in natural populations abounds, its genetic basis is rarely understood (Barton and Turelli, 1989; Flint and Mott, 2001).”

“…in manipulative experimental approaches, such as artificial selection and the measurement of correlated responses (Mitchell-Olds and Shaw 1987; Barton and Turelli 1989; Fry 1993; Brakefield and Roskam 2006; Roff 2007; for examples see Palmer and Dingle 1986; Bradshaw and Holzapfel 1996;…”

“Theoretical work has shown that a selection –migration balance can restore genetic variation in fitness related traits (reviewed in Felsenstein 1976, Slatkin 1987, Barton and Turelli 1989 ).”

“…1) (i > 1, t > 0) , (26) 7Because the newly-mutated population is a Gaussian of width determined by m2 for any distribution, this approximation is equivalent to the “house-of-cards” approximation introduced by (Kingman, 1978) and investigated in (Turelli, 1984), (Barton & Turelli, 1989).”

“One possibility is that climatic selection has recently depleted this variation, which can happen after just a few generations of strong selection (Barton, 1989).”