The sex locus is tightly linked to factors conferring sex-specific lethal effects in the mosquito Aedes aegypti

Abstract

In many taxa, sex chromosomes are heteromorphic and largely non-recombining. Evolutionary models predict that spread of recombination suppression on the Y chromosome is fueled by the accumulation of sexually antagonistic alleles in close linkage to the sex determination region. However, empirical evidence for the existence of sexually antagonistic alleles is scarce. In the mosquito Aedes aegypti, the sex-determining chromosomes are homomorphic. The region of suppressed recombination, which surrounds the male-specific sex-determining gene, remains very small, despite ancient origin of the sex chromosomes in the Aedes lineage. We conducted a genetic analysis of the A. aegypti chromosome region tightly linked to the sex locus. We used a strain with an enhanced green fluorescent protein (EGFP)-tagged transgene inserted near the male-determining gene to monitor crossing-over events close to the boundary of the sex-determining region (SDR), and to trace the inheritance pattern of the transgene in relation to sex. In a series of crossing experiments involving individuals with a recombinant sex chromosome we found developmental abnormalities leading to 1:2 sex biases, caused by lethality of half of the male or female progeny. Our results suggest that various factors causing sex-specific lethal effects are clustered within the neighborhood of the SDR, which in the affected sex are likely lost or gained through recombination, leading to death. These may include genes that are recessive lethal, vital for development and/or sexually antagonistic. The sex chromosome fragment in question represents a fascinating test case for the analysis of processes that shape stable boundaries of a non-recombining region.

A functional requirement for sex-determination M/m locus region lncRNA genes in Aedes aegypti female larvae

“…Although the A. aegypti M and m sex chromosomes are homomorphic, the sex-differentiated region extends to a ~ 100 Mb region that surrounds the ~ 1.5 Mb M locus 7 . Rare recombination events in the M locus region, in which recombination is typically suppressed, result in sex ratio distortion 8 , 9 . These distortions suggest that clusters of loci which cause sex-specific effects reside within the sex-determining region and are gained or lost through crossover events, causing sex-specific lethality 8 , 9 .…”

“…Rare recombination events in the M locus region, in which recombination is typically suppressed, result in sex ratio distortion 8 , 9 . These distortions suggest that clusters of loci which cause sex-specific effects reside within the sex-determining region and are gained or lost through crossover events, causing sex-specific lethality 8 , 9 . The factors, which may include genes that are vital for development or which are sexually antagonistic, may be shaping the stable boundaries of non-recombining sex chromosomes during A. aegypti sex chromosome evolution 9 , but the identities of these loci are unknown.…”

Diet effects on mouse meiotic recombination: a warning for recombination studies

“…In spite of this control, several studies have shown that environmental factors such as temperature changes (Bomblies et al 2015;Lloyd et al 2018;Plough 1917), stress (Belyaev and Borodin 1982), endocrine disruptors (Susiarjo et al 2007;Vrooman et al 2015) and infections (Singh 2019) are able to modify the recombination rate. Even if these recombination changes may not be large enough to compromise fertility, they could have important consequences in the transmission and evolution of traits, as well as in genetic mapping studies (Dumont and Payseur 2008;Krzywinska et al 2016;Pardo-Manuel de Villena et al 2000;Ritz et al 2017). To date, only one analysis in flies has reported an effect of nutrition on crossover rate (Mostoufi 2021;Neel 1941), an effect that has also been suggested in yeast (Abdullah and Borts 2001).…”

Quiescence in Aedes aegypti: Interpopulation Differences Contribute to Population Dynamics and Vectorial Capacity

“…These results are consistent with previous reports [ 22 , 59 ]. Recent research has confirmed that sex determination in A. aegypti does not involve an XY chromosome but an endogenous meiotic driver system that can cause sexual proportion distortion with a predominance of males over females [ 60 , 61 ].…”