Disentangling Verbal Arguments: Intralocus Sexual Conflict in Haplodiploids

Abstract

In haplodiploids, (1) alleles spend twice as many generations in females as in males, (2) males are never heterozygous and therefore express recessive alleles, and (3) males sire daughters, but no sons. Intralocus sexual conflict therefore operates differently in haplodiploids than in diploids, and shares strong similarities with loci on X (or Z) chromosomes. The common co-occurrence of all three features makes it difficult to pinpoint their respective roles. However, they do not always co-occur in nature, and missing cases can be additionally studied with hypothetical life cycles. We model sexually antagonistic alleles in eight different sex determination systems, and find that arguments (1) and (2) promote invasion and fixation of female-beneficial and male-beneficial alleles, respectively; (2) also improves prospects for polymorphism. Argument (3) harms the invasion prospects of sexually antagonistic alleles (irrespective of which sex benefits), but promotes fixation should invasion nevertheless occur. Disentangling the features helps to evaluate the validity of previous verbal arguments and yields better informed predictions about intralocus sexual conflict under different sex determination systems, including hitherto undiscovered ones.

Sexual antagonism in haplodiploids

“…For a male-beneficial allele, the invasion conditions will be S > 2h f T and h m S > 2h f T under arrhenotoky and male PGE, respectively (full methods can be found in SM 2.1-2.2). Note that results for arrhenotoky are identical to the invasion conditions for Xlinked alleles with full dosage compensation (Rice 1984;Patten 2019), and assuming equal dominance (h f = h m ) also recovers the invasion conditions for PGE reported by Klein et al (2021). Under arrhenotoky (as with X-linked genes), the twofold weighting placed on females will be cancelled out by the twofold larger fitness effects in males (assuming h f = 1/2).…”

“…Sexual antagonism is one such example, whereby genetic variants may prove beneficial to one sex but detrimental to the other. This has motivated a large body of theoretical work considering when such sexually antagonistic alleles will be able to invade (Owen 1953), how this may vary across the genome (Parsons 1961;Kidwell et al 1977;Pamilo 1979;Rice 1984;Frank and Hurst 1996;Frank and Patten 2020;Hitchcock and Gardner 2020;Klein et al 2021), and how we may be able to detect such alleles from population genetic data (Cheng and Kirkpatrick 2016;Kasimatis et al 2019;. This theory has been complemented more recently by molecular and quantitative genetic studies of laboratory and wild populations, both estimating the extent of sexual antagonism, and identifying specific loci at which sexu-ally antagonistic alleles reside (Poissant et al 2010;Mank 2017;Rowe et al 2018;Connallon and Matthews 2019).…”

“…First, mechanisms of dosage compensation-that ensure an equal balance of X-linked versus autosomal gene products between females and males-are understood to play an important role in modulating sexual antagonism in relation to the X chromosome (Hitchcock and Gardner 2020), but it is unclear whether these mechanisms should apply in the same way in relation to arrhenotokous species in which males are haploid across their entire genome, and thus, might be able to achieve dosage compensation either passively, or through other mechanisms (e.g., additional endoreduplication) (Aron et al 2005;Scholes et al 2013). Second, although PGE is similar to X-linkage from a transmission perspective, this form of haplodiploidy involves males being somatically diploid through some or all of their lives (Burt and Trivers 2006;Gardner and Ross 2014;Klein et al 2021), with concomitant gene dosage and dominance effects that may be expected to affect the balance between female-versus male-beneficial alleles.…”

“…1977; Pamilo 1979; Rice 1984; Frank and Hurst 1996; Frank and Patten 2020; Hitchcock and Gardner 2020; Klein et al. 2021), and how we may be able to detect such alleles from population genetic data (Cheng and Kirkpatrick 2016; Kasimatis et al. 2019; Ruzicka and Connallon 2020; Ruzicka et al.…”

“…Second, although PGE is similar to X‐linkage from a transmission perspective, this form of haplodiploidy involves males being somatically diploid through some or all of their lives (Burt and Trivers 2006; Gardner and Ross 2014; Klein et al. 2021), with concomitant gene dosage and dominance effects that may be expected to affect the balance between female‐ versus male‐beneficial alleles.…”