Heterochiasmy and Sexual Dimorphism: The Case of the Barn Swallow (Hirundo rustica, Hirundinidae, Aves)

Abstract

Heterochiasmy, a sex-based difference in recombination rate, has been detected in many species of animals and plants. Several hypotheses about evolutionary causes of heterochiasmy were proposed. However, there is a shortage of empirical data. In this paper, we compared recombination related traits in females and males of the barn swallow Hirundo rustica (Linnaeus, 1758), the species under strong sexual selection, with those in the pale martin Riparia diluta (Sharpe and Wyatt, 1893), a related and ecologically similar species with the same karyotype (2N = 78), but without obvious sexual dimorphism. Recombination traits were examined in pachytene chromosome spreads prepared from spermatocytes and oocytes. Synaptonemal complexes and mature recombination nodules were visualized with antibodies to SYCP3 and MLH1 proteins, correspondingly. Recombination rate was significantly higher (p = 0.0001) in barn swallow females (55.6 ± 6.3 recombination nodules per autosomal genome), caused by the higher number of nodules at the macrochromosomes, than in males (49.0 ± 4.5). They also showed more even distribution of recombination nodules along the macrochromosomes. At the same time, in the pale martin, sexual differences in recombination rate and distributions were rather small. We speculate that an elevated recombination rate in the female barn swallows might have evolved as a compensatory reaction to runaway sexual selection in males.

Pangenomics provides insights into the role of synanthropy in barn swallow evolution

“…The chromosome reconstruction (2n = 80) matches our cytogenetic analysis (Fig. 1a; Additional file 1: Supplementary Note), and is in line with the current literature on pachytene karyotypes of the barn swallow (41). Based on the original chicken chromosome classification (42) and our chromosome sizes (Additional file 1: Table S3, Supplementary Note), we define chromosomes 1-6 and Z as macrochromosomes, 7-13 and W as intermediate-size chromosomes, and 14-39 as microchromosomes.…”

The genetic architecture of recombination rates is polygenic and differs between the sexes in wild house sparrows (Passer domesticus)

“…Phylogeny of birds where within sex recombination rates have been estimated using linkage mapping, or cytogenetic analysis of chiasma counts using MLH1 foci or recombination nodules (indicated by *). The underlying data is provided in Table S5 using data compiled in (Malinovskaya et al . 2020b) and other sources.…”

Sex‐linked genetic diversity and differentiation in a globally distributed avian species complex

“…Related to this point, Z‐linked regions recombine only in males, requiring a potentially extreme male recombination bias for the effective recombination rate of the Z to match that of autosomes. However, a recent study found intriguing evidence for female‐biased recombination rates in barn swallows (Malinovskaya et al, 2020). While we did not estimate recombination rates here, these factors together argue that low rates of recombination on the Z chromosome contribute to low genetic diversity through linked selection.…”