Stress-induced recombination and the mechanism of evolvability

Abstract

16The concept of evolvability is controversial. To some, it is simply a measure of the standing genetic 2 17 variation in a population and can be captured by the narrowsense heritability (h ). To others, 18 evolvability refers to the capacity to generate heritable phenotypic variation. Many scientists, 19 including Darwin, have argued that environmental variation can generate heritable phenotypic 20 variation. However, their theories have been difficult to test. Recent theory on the evolution of sex 21 and recombination provides a much simpler framework for evaluating evolvability. It shows that 22 modifiers of recombination can increase in prevalence whenever low fitness individuals produce 23 proportionately more recombinant offspring. Because recombination can generate heritable variation, 24 stressinduced recombination might be a plausible mechanism of evolvability if populations exhibit a 25 negative relationship between fitness and recombination. Here we use the fruit fly, Drosophila 26melanogaster, to test for this relationship. We exposed females to mating stress, heat shock or cold 27 shock and measured the temporary changes that occurred in reproductive output and the rate of 28 chromosomal recombination. We found that each stress treatment increased the rate of recombination 29 and that heat shock, but not mating stress or cold shock, generated a negative relationship between 30 reproductive output and recombination rate. The negative relationship was absent in the lowstress 31 controls, which suggests that fitness and recombination may only be associated under stressful 32 conditions. Taken together, these findings suggest that stressinduced recombination might be a 33 mechanism of evolvability. 34 35

Widely distributed hot and cold spots in meiotic recombination as shown by the sequencing of rice F2 plants

“…Our data have clearly shown that environmental stress can indeed increase the recombination rate in some stress‐treated individuals, although not all of the offspring whose parent was treated by stress showed a higher number of crossover events (Table ); this is consistent with previous expectations and reports indicating that environmental variations can contribute to evolution through the generation of novel heritable variations via meiotic and somatic recombination (Darwin, ; Puchta et al ., ; Lucht et al ., ; Kovalchuk et al ., ; Molinier et al ., ; Zhang, ; Zhong & Priest, ; Kerstes et al ., ; Puchta & Hohn, ). Interestingly, not all of the stress‐treated individuals have a greater number of crossover events, and only a 1.5‐fold higher recombination rate was found in individuals with the highest recombination rate (52) compared with the average rate (34) (Table ).…”

“…Previous studies have argued that environmental variations may contribute to evolution through the generation of novel heritable variations via adaptive mutations and/or recombination (Darwin, ; Zhang, ). In addition, a number of studies have shown that many abiotic and biotic factors, such as high salinity, UV irradiation, temperature and pathogen attack, etc., can directly increase somatic recombination, a finding which has been confirmed by the detection of marker transgene‐dependent Arabidopsis lines with imposed stress treatment (Puchta et al ., ; Lucht et al ., ; Kovalchuk et al ., ; Molinier et al ., ; Francis et al ., ; Zhong & Priest, ; Kerstes et al ., ; Puchta & Hohn, ). Moreover, in Drosophila , hot and cold temperatures can also induce higher recombination rates (Smith, ).…”

Dispersing away from bad genotypes: the evolution of Fitness-Associated Dispersal (FAD) in homogeneous environments

“…The concept of Fitness associated dispersal is part of the more general concept of fitness-associated genetic variation generated through mutation [70,71], recombination in a mixed population [55,72,73], and in particular costly variation, such as condition-dependent sex [56,57,74]. The marked difference between condition-dependent sex and FAD is that, in condition-dependent sex, individuals that do not meet the conditions to reproduce sexually produce offspring that are identical to themselves.…”

Condition-dependent sex: who does it, when and why?

“…In flies, a negative relationship between fitness and recombination rate was observed for heat and pathogen stress, but not for mating or cold stress [80][81][82], and deleterious mutations have been shown to alter the recombination rate, but not in a consistent way [83].…”