A genetic linkage map for the salmon louse (Lepeophtheirus salmonis): evidence for high male:female and inter-familial recombination rate differences

Abstract

A salmon louse (Lepeophtheirus salmonis salmonis) genetic linkage map was constructed to serve as a genomic resource for future investigations into the biology of this important marine parasitic copepod species, and to provide insights into the inheritance patterns of genetic markers in this species. SNP genotyping of 8 families confirmed the presence of 15 linkage groups based upon the assignment of 93,773 markers. Progeny sample size weight adjusted map sizes in males (with the exception of SL12 and SL15) ranged in size from 96.50 cM (SL11) to 134.61 cM (SL06), and total combined map steps or bins ranged from 143 (SL09) to 203 (SL13). The SL12 male map was the smallest linkage group with a weight-averaged size of 3.05 cM with 6 recombination bins. Male:female specific recombination rate differences are 10.49:1 and represent one of the largest reported sex-specific differences for any animal species. Recombination ratio differences (M:F) ranged from 1.0 (SL12) to 29:1 (SL15). The number of markers exhibiting normal Mendelian segregation within the sex linkage group SL15 was extremely low (N = 80) in comparison to other linkage groups genotyped [range: 1459 (SL12)-10206 markers (SL05)]. Re-evaluation of Mendelian inheritance patterns of markers unassigned to any mapping parent according to hemizygous segregation patterns (models presented) identified matches for many of these markers to hemizygous patterns. The greatest proportion of these markers assigned to SL15 (N increased to 574). Inclusion of the hemizygous markers revised SL15 sexspecific recombination rate differences to 28:1. Recombination hot-and coldspots were identified across all linkage groups with all linkage groups possessing multiple peaks. Nine of 13 linkage groups evaluated possessed adjacent domains with hot-coldspot transitional zones. The most common pattern was for one end of the linkage to show elevated recombination in addition to internal regions. For SL01 and SL06, however, a terminal region with high recombination was not evident while a central domain possessing extremely high-recombination levels was present. High levels of recombination were weakly coupled to higher levels of SNP variation within domains, but this association was very strong for the central domains of SL01 and SL06. From the pooled paternal half-sib lots (several virgin females placed with 1 male), only 1 or two surviving family lots were obtained. Surviving families possessed parents where both the male and female possessed either inherently low or high recombination rates. This study provides insight into the organization of the sea louse genome, and describes large differences in recombination rate that exist among individuals of the same sex, and between the sexes. These differences in recombination rate may be coupled to the capabilities of this species to adapt to environmental and pharmaceutical treatments, given that family survivorship appears to be enhanced when parents have similar recombination levels.

The salmon louse genome: copepod features and parasitic adaptations

“…A single scaffold assigned to LG15 received average mapping from both males and females suggesting it to represent a homologous region shared between the Z and W chromosomes. These findings agree with the conclusions drawn by [53].…”

“…A lack of heterozygous markers was observed in LG15 in females, whereas heterozygosity was common in males for the same LG (Fig. 2B) confirming that LG15 is a sex chromosome as previously suggested [53]. These observations functionally explain the 1:1 male:female ratio in salmon lice and are compatible with both a ZZ-ZW and a ZZ-Z0 sex chromosome configuration and alternative chromosome configurations with several sex chromosomes as previously reported in both deuterostome and protostome animals [78, 79].…”

“…Interestingly, in similarity to the D. melanogaster ‘dot’ chromosome, the salmon louse also has a chromosome sheltered from recombination in both sexes; the chromosome corresponding to LG12 (Fig. 2 and [53]).…”

“…SNPs were then assigned to chromosomes with the SeparateChromosomes2 function. The default parameter of SeparateChromosomes2 lead to 13 autosomes, but previous work based on a larger number of markers [53], showed that the genome of L. salmonis comprises 14 autosomes. The SeparateChromosomes2 function was therefor run again with a higher threshold parameter (), identifying 14 autosomes and one sex chromosome.…”

The salmon louse genome may be much larger than sequencing suggests

“…The salmon louse genome has been sequenced several times using various sequencing platforms, and six independent genome assemblies have been made -including two chromosome level assemblies (Table 1). The resulting assemblies appear consistent in structure, as revealed by linkage analyses [33,40,46], and sizes (Table 1), collectively suggesting the salmon louse genome size to be approximately 600-700 Mbps.…”