Abstract
The Anopheles gambiae complex is comprised of eight morphologically indistinguishable species and has emerged as a model system for the study of speciation genetics due to the rapid radiation of its member species over the past two million years. Male hybrids between most An. gambiae complex species pairs are sterile, and some genotype combinations in hybrid males cause inviability. We investigated the genetic basis of hybrid male inviability and sterility between An. coluzzii and An. quadriannulatus by measuring segregation distortion and performing a QTL analysis of sterility in a backcross population. Hybrid males were inviable if they inherited the An. coluzzii X chromosome and were homozygous at one or more loci in 18.9 Mb region of chromosome 3. The An. coluzzii X chromosome has a disproportionately large effect on hybrid sterility when introgressed into an An. quadriannulatus genetic background. Additionally, an epistatic interaction between the An. coluzzii X and a 1.12 Mb, pericentric region of the An. quadriannulatus 3L chromosome arm has a statistically significant contribution to the hybrid sterility phenotype. This same epistatic interaction occurs when the An. coluzzii X is introgressed into the genetic background of An. arabiensis, the sister species of An. quadriannulatus, suggesting that this may represent one of the first Dobzhansky–Muller incompatibilities to evolve early in the radiation of the Anopheles gambiae species complex. We describe the additive effects of each sterility QTL, epistatic interactions between them, and genes within QTL with protein functions related to mating behavior, reproduction, spermatogenesis, and microtubule morphogenesis, whose divergence may contribute to post-zygotic reproductive isolation between An. coluzzii and An. quadriannulatus.
Highlights
The study of speciation genetics and genomics has largely focused on the evolution of hybrid dysfunction (Dobzhansky, 1937; Coyne and Orr, 2004) because it represents the first step in the formation of post-zygotic reproductive isolation between diverging populations
We identified regions of the An. coluzzii genome that result in hybrid inviability when introgressed into an An. quadriannulatus genetic background by analyzing segregation distortion of autosomal loci in the An. quadriannulatus X chromosome and An. coluzzii X chromosome datasets
The larger relative genetic map of the second chromosome is likely due to the presence of the 2La inversion, which is fixed between these species and can significantly increase recombination frequency on the 2R (i.e., Schultz-Redfield Effect, Schultz and Redfield, 1951; Lucchesi and Suzuki, 1968; Stevison et al, 2011), and segregation distortion resulting from male inviability for some genotype combinations (Hackett and Broadfoot, 2003; Zuo et al, 2019)
Summary
The study of speciation genetics and genomics has largely focused on the evolution of hybrid dysfunction (Dobzhansky, 1937; Coyne and Orr, 2004) because it represents the first step in the formation of post-zygotic reproductive isolation between diverging populations. Post-Zygotic Reproductive Isolation Between Anopheles coluzzii and An. quadriannulatus two putative species, and is impacted by the number of mutations separating two allopatric lineages at any given time, the number of incompatibilities per mutation, and the fitness of each incompatibility (Orr and Turelli, 2001). Upon secondary contact of genetically divergent populations, epistatic loci on parental chromosomes are unable to function effectively in hybrids. The snowball effect has been supported by empirical evidence of the rate of DMI evolution between Drosophila (Matute et al, 2010; Matute and Gavin-Smyth, 2014) and Solanum sibling species pairs (Moyle and Nakazato, 2010)
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