Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2018 Aug;209(4):1329-1344.
doi: 10.1534/genetics.118.300894. Epub 2018 Jun 6.

The Genomic Architecture of a Rapid Island Radiation: Recombination Rate Variation, Chromosome Structure, and Genome Assembly of the Hawaiian Cricket Laupala

Affiliations
Free PMC article

The Genomic Architecture of a Rapid Island Radiation: Recombination Rate Variation, Chromosome Structure, and Genome Assembly of the Hawaiian Cricket Laupala

Thomas Blankers et al. Genetics. .
Free PMC article

Abstract

Phenotypic evolution and speciation depend on recombination in many ways. Within populations, recombination can promote adaptation by bringing together favorable mutations and decoupling beneficial and deleterious alleles. As populations diverge, crossing over can give rise to maladapted recombinants and impede or reverse diversification. Suppressed recombination due to genomic rearrangements, modifier alleles, and intrinsic chromosomal properties may offer a shield against maladaptive gene flow eroding coadapted gene complexes. Both theoretical and empirical results support this relationship. However, little is known about this relationship in the context of behavioral isolation, where coevolving signals and preferences are the major hybridization barrier. Here we examine the genomic architecture of recently diverged, sexually isolated Hawaiian swordtail crickets (Laupala). We assemble a de novo genome and generate three dense linkage maps from interspecies crosses. In line with expectations based on the species' recent divergence and successful interbreeding in the laboratory, the linkage maps are highly collinear and show no evidence for large-scale chromosomal rearrangements. Next, the maps were used to anchor the assembly to pseudomolecules and estimate recombination rates across the genome to test the hypothesis that loci involved in behavioral isolation (song and preference divergence) are in regions of low interspecific recombination. Contrary to our expectations, the genomic region where a male song and female preference QTL colocalize is not associated with particularly low recombination rates. This study provides important novel genomic resources for an emerging evolutionary genetics model system and suggests that trait-preference coevolution is not necessarily facilitated by locally suppressed recombination.

Keywords: chromosomal rearrangements; crickets; genome; recombination; sexual selection; speciation.

Figures

Figure 1
Figure 1
Study design. (A) The phylogenetic relationships of studied Laupala species based on a neighbor-joining tree generated from genetic distances among the parental lines used in this study. Dashed gray lines connect species pairs that were crossed. (B) Approximate distributions of the studied species on the Big Island of Hawaii. (C) Hypothetical segregation and linkage map construction for five genetic loci A, B, C, D, and E in three crosses of four species. The genetic distance between the loci is 5 cM in each of the four species. Loci [B, C, D] are inverted in the green and black species. When two species that have alternative karyotypes for the inversion are crossed (pair 2), loci in the inversion will not recombine in the first-generation hybrid, resulting in reduced genetic (map) length in the second-generation hybrid. Other chromosomal rearrangements will have similar effects. Only if two crosses involve homokaryotypic species pairs that have alternative karyotypes can an inversion be detected in a comparison of intercross linkage maps.
Figure 2
Figure 2
Initial linkage maps. Bars represent LGs for ParKoh, KonPar, and PruKoh. Lines within the bars indicate marker positions. The scale on the left measures marker spacing in cM. Blue lines connect markers on the same scaffold between the different maps. The map for ParKoh is shown twice to facilitate comparison across all three maps. See Figure S1 for comprehensive maps.
Figure 3
Figure 3
Segregation distortion. For each of the seven autosomal LGs within the three comprehensive linkage maps (from top to bottom: ParKoh, KonPar, and PruKoh), a sliding window of the negative log-transformed P-values for the χ2-square test for deviation from a 1:2:1 segregation ratio is shown across markers with black lines in the top panels. In the panel below, the trace of the frequency of heterozygote genotypes (blue lines) and homozygote genotypes for both parental alleles (black and red lines, respectively) is shown. For each intercross, dashed gray lines indicate P = 0.01 (top panels) or expected allele frequencies based on 1:2:1 inheritance (bottom panels).
Figure 4
Figure 4
Recombination and Marey maps. Grayscale symbols and lines indicate the relationship between the physical distance (scaffold midposition) in Mb on the x-axis and the genetic distance in cM for each of the eight LGs on the left y-axis. ○’s represent the dense ParKoh linkage map, ▵’s and ⋄’s represent that of the KonPar and PruKoh cross, respectively. The corresponding lines (ParKoh: solid; KonPar: dashed; PruKoh: dotted) indicate the fitted smoothing spline (10 d.f.). The red lines (same stroke style) show the first order derivative of the fitted splines and represent the variation in recombination rate as a function of physical distance (cM/Mb, on the right y-axis). Gray bars indicate the approximate location of male song rhythm QTL peaks. The yellow ☆ in the LG1 panel highlights the QTL peak that colocalizes with a female preference QTL peak (Shaw and Lesnick 2009).

Similar articles

See all similar articles

Cited by 5 articles

Publication types

LinkOut - more resources

Feedback