Increased recombination frequencies resulting from directional selection for geotaxis in Drosophila

Abstract

Several classes of models have been suggested to explain how natural selection can favour non-zero recombination. Directional and fluctuating selection, abiotic and biotic, and selection against harmful mutations seem to be the most plausible factors, but little has been done to test the problem experimentally. Here we show that long-term selection for positive or negative geotaxis in Drosophila melanogaster results in a dramatic increase in recombination rates in different genomic regions. The total increment in recombination for the genome portion considered is 78 cM for geo + and 66 cM for geo -. Selectionfor negative geotaxis did not result in recombination changes in chromosome 2 whereas selection in the opposite direction caused nearly a four-fold increase in the b-cn segment and a significant, albeit not as high, increase in the adjacent regions, al-b and cn-vg. In chromosomes X and 3, a significant increase in recombination was found in both selected lines. In total, the increment in exchange frequency in chromosome X (y-cv-ct-v-car) was from 72.6 per cent (the control level) to 124.7 and 110.3 per cent geo -and geo , respectively, whereas for the studied portion of chromosome 3 (ru-h-cu-sr-e) we obtained, correspondingly, 60.8, 76.4 and 73.8 per cent. Thus, in general, selection for geotaxis resulted in increased recombination frequencies regardless of the direction of selection. These results, taken together with other data, allow one to conclude that selection for fitness traits (e.g. for changed levels of quantitative traits, behavioural peculiarities or adaptation to adverse environmental conditions) may be a powerful factor causing rather rapid changes in the recombination system.

Variation in genomic recombination rates among animal taxa and the case of social insects

“…Domestication is typically associated with strong directional selection exerted by breeders, which is known to increase recombination rates (e.g., in Korol and Iliadi, 1994). Increased values of recombination, as measured by chiasmata frequencies, have, in fact, been observed in domesticated mammals (Burt and Bell, 1987) and plants ( Ross-Ibarra, 2004).…”

Genetic recombination and adaptation to fluctuating environments: selection for geotaxis in Drosophila melanogaster

“…This genetic analysis is consistent with the results obtained in a study that looked at the effects of selection on recombination rates. Korol and Iliadi (1994) selected both positively and negatively for geotaxis in D. melanogaster and observed substantial increases in recombination. Across all regions studied, the map length rose from 217.0 cM in the control line to 295.9 and 283.4 cM in the lines selected for negative and positive geotaxis over a period of 50 generations, respectively.…”

“…This has been verified in a number of empirical studies (eg Harinarayana and Murty, 1971;Flexon and Rodell, 1982;Zhuchenko et al, 1985;Burt and Bell, 1987;Wolf et al, 1987;Korol and Iliadi, 1994). The reverse predictionthat is that manipulating the level of recombination should result in changes in the response to selectionhas received some attention to date, with contradictory results (Carson, 1958;McPhee and Robertson, 1970;Markow, 1975;Malmberg, 1977;Thompson, 1977;Zeyl and Bell, 1997;Rice and Chippendale, 2001).…”

Ecological stress and sex evolution in soil microfungi

“…Lond. B (2003) theoretical analysis have shown that directional selection, in combination with nite population size and/or spatial heterogeneity, may promote a selective advantage of increased recombination under much less restrictive assumptions than usually thought (Flexon & Rodell 1982;Gorodetski et al 1990;Korol & Iliadi 1994;Otto & Barton 1997;Korol 1999;Lenormand & Otto 2000). Assuming that sex helps organisms to adapt to adverse conditions, one can further propose that in natural populations of fungi the abundance of sexual forms will be positively correlated with the severity of stress.…”