Strong hybrid male incompatibilities impede the spread of a selfish chromosome between populations of a fly



Verspoor, Rudi L, Smith, Jack ML, Mannion, Natasha LM, Hurst, Gregory DD ORCID: 0000-0002-7163-7784 and Price, Tom AR ORCID: 0000-0002-4394-6301
(2018) Strong hybrid male incompatibilities impede the spread of a selfish chromosome between populations of a fly. Evolution Letters, 2 (3). 169 - 179.

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Abstract

Meiotically driving sex chromosomes manipulate gametogenesis to increase their transmission at a cost to the rest of the genome. The intragenomic conflicts they produce have major impacts on the ecology and evolution of their host species. However, their ecological dynamics remain poorly understood. Simple population genetic models predict meiotic drivers will rapidly reach fixation in populations and spread across landscapes. In contrast, natural populations commonly show spatial variation in the frequency of drivers, with drive present in clines or mosaics across species ranges. For example, Drosophila subobscura harbors a sex ratio distorting drive chromosome (SRs) at 15–25% frequency in North Africa, present at less than 2% frequency in adjacent southern Spain, and absent in other European populations. Here, we investigate the forces preventing the spread of the driver northward. We show that SRs has remained at a constant frequency in North Africa, and failed to spread in Spain. We find strong evidence that spread is impeded by genetic incompatibility between SRs and Spanish autosomal backgrounds. When we cross SRs from North Africa onto Spanish genetic backgrounds we observe strong incompatibilities specific to hybrids bearing SRs. The incompatibilities increase in severity in F2 male hybrids, leading to almost complete infertility. We find no evidence supporting an alternative hypothesis, that there is resistance to drive in Spanish populations. We conclude that the source of the stepped frequency variation is genetic incompatibility between the SRs chromosome and the genetic backgrounds of the adjacent population, preventing SRs spreading northward. The low frequency of SRs in South Spain is consistent with recurrent gene flow across the Strait of Gibraltar combined with selection against the SRs element through genetic incompatibility. This demonstrates that incompatibilities between drive chromosomes and naïve populations can prevent the spread of drive between populations, at a continental scale.

Item Type: Article
Uncontrolled Keywords: compatibility, Drosophila subobscura, segregation-distortion, selfish genetic elements, suppression, X chromosome meiotic drive
Depositing User: Symplectic Admin
Date Deposited: 20 Jun 2018 14:14
Last Modified: 27 Nov 2021 06:10
DOI: 10.1002/evl3.55
Open Access URL: https://doi.org/10.1002/evl3.55
Related URLs:
URI: https://livrepository.liverpool.ac.uk/id/eprint/3022840