A high density linkage map reveals sexual dimorphism in recombination landscapes in red deer (Cervus elaphus)

Abstract

6High density linkage maps are an important tool to gain insight into the genetic architecture of 7 traits of evolutionary and economic interest, and provide a resource to characterise variation 8 in recombination landscapes. Here, we used information from the cattle genome and the 50K 9Cervine Illumina BeadChip to inform and refine a high density linkage map in a wild population 10 of red deer (Cervus elaphus). We constructed a predicted linkage map of 38,038 SNPs and a 11 skeleton map of 10,835 SNPs across 34 linkage groups. We identified several chromosomal 12 rearrangements in the deer lineage relative to sheep and cattle, including six chromosome fis-13 sions, one fusion and two large inversions. Otherwise, our findings showed strong concordance 14 with map orders in the cattle genome. The sex-averaged linkage map length was 2739.7cM 15 and the genome-wide autosomal recombination rate was 1.04cM per Mb. The female autoso-16 mal map length was 1.21 longer than that of males (2767.4cM vs 2280.8cM, respectively). Sex 17 differences in map length were driven by high female recombination rates in peri-centromeric 18 regions, a pattern that is unusual relative to other mammal species. This effect was more 19 pronounced in fission chromosomes that would have had to produce new centromeres. We 20 propose two hypotheses to explain this effect: (1) that this mechanism may have evolved to 21 counteract centromeric drive associated with meiotic asymmetry in oocyte production; and/or 22 (2) that sequence and structural characteristics suppressing recombination in close proximity 23 to the centromere may not have yet evolved at neo-centromeres. Our study provides insight 24 into how recombination landscapes vary and evolve in mammals, and will provide a valuable 25 1 . CC-BY-ND 4.0 International license not peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was . http://dx.doi.org/10.1101/100131 doi: bioRxiv preprint first posted online Jan. 13, 2017; resource for studies of evolution, genetic improvement and population management in red deer 26 and related species. 27 Article Summary 28We present a high density linkage map (>38,000 markers) in a wild population of Red deer 29 (Cervus elaphus). Our investigation of the recombination landscape showed a marked differ-30 ence in recombination rates between the sexes in proximity to the centromere, with females 31showing an unusually elevated rate relative to other mammal species. This effect is most pro-32 nounced in chromosomes that would have produced a new centromere in the deer lineage. We 33propose that the observed effects have evolved to counteract selfish genetic elements associ-34 ated with asymmetrical female meiosis. 35

Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics

“…Our insights from the analysis among species were further reinforced by relating CO rate to chromosome length within species. In both animals and plants, the correlation between these two variables was generally strongly negative among chromosomes (Figure b; the distribution of correlation coefficients was not visualized for fungi because only two species were available, but both species also showed a negative coefficient; see also Backström et al., ; Giraut et al., ; International Human Genome Sequencing Consortium ; Jensen‐Seaman et al., ; Johnston, Huisman, Ellis, & Pemberton, ; Kaback, Guacci, Barber, & Mahon, ; Roesti et al., ; Smeds et al., ; Tortereau et al., ).…”

“…Another potentially important aspect is crossover interference, that is, the inhibition of additional CO in the vicinity of an existing CO along a chromosome (Muller, ; Sturtevant, ). This is suggested by sexual dimorphism in the distribution of CO: remarkably consistently across species, the enrichment of CO near the telomeres is more pronounced in the male than the female sex (Broman, Murray, Sheffield, White, & Weber, ; Cox et al., ; Giraut et al., ; Johnston et al., , ; Lien et al., ; Ma et al., ; Smeds et al., ). Interestingly, the sexes also appear to differ in the structural organization of meiotic chromosomes, with the paired homologous chromosomes being less condensed in oocytes than spermatocytes (Tease & Hulten, ).…”

Increased genetic marker density reveals high levels of admixture between red deer and introduced Japanese sika in Kintyre, Scotland

“…However, during the development of the chip 2,250 SNPs were included that were expected to be diagnostic between red deer and sika, and 2,250 SNPs were included that were expected to be diagnostic between red deer and wapiti. Within each marker set, SNPs were selected to be evenly spaced throughout the genome according to map positions in the bovine genome, with which the deer genome has high homology (Johnston, Huisman, Ellis, & Pemberton, ; Slate et al, ). To check for consistency between batches and calculate the repeatability of each SNP, we used the same positive control twice on each 96‐well plate (Huisman et al, ).…”

A genome‐wide linkage map for the house sparrow (Passer domesticus) provides insights into the evolutionary history of the avian genome

“…Linkage maps were previously limited to humans ( Homo sapiens ) (Weissenbach et al, ) and model or life stock species such as mice ( Mus musculus ) (Copeland et al, ), sheep ( Ovis aries ) (Crawford et al, ), zebra finch (Backström et al, ) or Atlantic salmon ( Salmo salar ) (Lien et al, ). With the advancement of genotyping technology, linkage maps from many wild populations have become available, and include great reed warbler ( Acrocephalus arundinaceus ) (Åkesson, Hansson, Hasselquist, & Bensch, ), red deer ( Cervus elaphus ) (Johnston et al, ), collard flycatcher ( Ficedula albicollis ) (Kawakami et al, ), great tit ( Parus major ) (van Oers et al, ) and Soay sheep (Slate et al, ). These linkage maps greatly facilitate association studies in wild populations, often with the aim of mapping genes for ecologically important phenotypes.…”