Academic journal article Genetics

Genetics of Genome-Wide Recombination Rate Evolution in Mice from an Isolated Island

Academic journal article Genetics

Genetics of Genome-Wide Recombination Rate Evolution in Mice from an Isolated Island

Article excerpt

MEIOTIC recombination is a fundamental part of genetic transmission in most eukaryotes. The sets of chromosomes gametes receive undergo an exchange of genetic material through a process known as crossing over. Crossovers, long recognized cytologically as chiasmata (Janssens 1909), fuse alleles into new haplotypic combinations. Recombination thus forms a knob that tunes the speed with which haplotypic diversity enters a population. The settings on this knob-recombination rates-are heritable, and they vary between individuals, populations, and species (True et al. 1996; Kong et al. 2004; Coop et al. 2008; Smukowski and Noor 2011; Comeron et al. 2012; Ritz et al. 2017).

The production of genetic variation among offspring by meiotic recombination is theorized to provide an advantage to organismal fitness by improving the efficacy of selection (Weismann et al. 1891; Kondrashov 1993; Burt 2000). Many models attribute the evolutionary advantage of recombination to its ability to dispel negative, nonrandom allelic combinations in a population ("negative linkage disequilibrium") produced by epistatic interactions (Feldman et al. 1980; Barton 1995) or by genetic drift (Hill and Robertson 1966; Felsenstein 1974; Otto and Barton 1997). In this theoretical framing, the advantages of eliminating negative linkage disequilibrium lead to indirect selection favoring recombination. Increased recombination rate in response to artificial selection on a variety of phenotypes (Flexon and Rodell 1982; Burt and Bell 1987; Gorlov et al. 1992; Korol and Iliadi 1994) provides evidence supporting this hypothesis, though some studies reveal no such increase (Bourguet et al. 2003; Muñoz-Fuentes et al. 2015). In nature, indirect selection on recombination rate is likely to be strongest in populations subject to directional selection, including those populations experiencing new environments (Otto and Barton 2001).

Another possibility is that recombination rate itself is targeted by selection. Chiasmata generate physical tension between homologous chromosome pairs in meiosis, a necessity for proper chromosome disjunction (Roeder 1997; Hassold and Hunt 2001). This process leads to the constraint that each chromosome, or chromosome arm, harbor at least one crossover (Pardo-Manuel de Villena and Sapienza 2001; Fledel-Alon et al. 2009). It has also been suggested that the number of recombination events is limited to reduce the chances of aberrant exchange, which can lead to deleterious chromosomal rearrangements (Inoue and Lupski 2002; Coop and Przeworski 2007). In the laboratory, artificial selection targeting recombination rate often generates a response (Chinnici 1971; Kidwell and Kidwell 1976; Charlesworth and Charlesworth 1985). Furthermore, there is some evidence that human mothers with higher average rates of crossing over have more children (Kong et al. 2004; Coop et al. 2008).

Understanding how recombination rate differences are inherited illuminates the evolution of this key genomic parameter. Multiple loci that shape recombination rate variation have been identified (Murdoch et al. 2010; Dumont andPayseur2011a; Balcovaetal. 2016; Hunteretal. 2016), including variants in specific genes (Kong et al. 2008, 2014; Sandor etal. 2012; Ma etal. 2015; Johnston etal. 2016). In addition to confirming that recombination rate is a genetically complex trait with the capacity to respond to evolutionary forces, these findings provide a window into the evolutionary history of recombination rate. Current recombination rates capture only a single moment in evolutionary time, but each allele that increases or decreases recombination rate documents a genetic change in an ancestral population.

Despite this progress, the existing picture of the genetics of recombination rate variation suffers from important biases. First, loci have either been identified through genome-wide association studies within populations (Kong et al. 2008, 2014; Sandor et al. …

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