An advantage for the evolution of male haploidy and systems with similar genetic transmission

Abstract

SUMMARYIn arthropods and rotifers a variety of genetic systems share the common property that males transmit only their mother's genome while females transmit genomes of both parents. Many of these have long been recognised because of the haploidy of males, but there are also some species in which males are diploid and yet transmit only the maternal genome. It is shown that the evolution of these maternal-genome-transmitting males ("haploid" males) is governed by the simple selective principle that maternal alleles occur at twice the frequency in gametes of haploid sons as in gametes of diploid sons. Under a simple constraint on the fitness of haploid males, selection favours mothers which produce haploid sons merely because they transmit maternal alleles at a greater rate than do diploid sons. The advantage to mothers in producing haploid sons is at the expense of the paternal genome, which is not transmitted by haploid sons. There is therefore counter-selection on fathers to produce diploid sons, and if the right genetic variation arises this countering selection will revert male haploidy to diploidy. These arguments apply to large, randommating populations but not necessarily to inbred populations.

Sex determination in the Hymenoptera: a review of models and evidence

“…Bull (1981) The models of Hartl & Brown (1970) and Bull (1981) assume random mating. Inbreeding might facilitate the evolution of arrhenotoky by decreasing the frequency of recessive, deleterious genes (Bull, 1979;Borgia, 1980). However, inbreeding also leads to high diploid male production, which would likely outweigh any advantage due to reduced frequencies of deleterious recessives (Bull, 1981).…”

Evolution of pseudo-arrhenotoky

“…However, it has evolved independently at least three times in the arthropods and, because it is much less easy to detect than arrhenotoky and because it has not been investigated systematically, it might be much more widespread than is currently thought. According to Bull (1979Bull ( , 1983) the selective advantage for the evolution of male haploidy stems from a two-fold representation of maternal genes in gametes of haploid sons in comparison to diploid sons of biparental origin. The probability of gene identity-by-descent between grandmother and grandchild through uniparental sons is therefore double the probability through biparental sons.…”

“…This two-fold advantage of producing uniparental sons may overcome the potential lower fitness of these sons and may therefore be the key to our understanding of the advantage of male haploidy. As noted by Bull (1979Bull ( , 1983 ) the two-fold advantage provides a selective basis not only for male haploidy but also for the evolution of any genetic system in which the genes of one parent are excluded from gametes in the offspring of one sex. Bull (1979Bull ( , 1983 therefore considered four different systems with two sexes in which offspring of one sex transmit only the genome inherited from one parent.…”

“…As noted by Bull (1979Bull ( , 1983 ) the two-fold advantage provides a selective basis not only for male haploidy but also for the evolution of any genetic system in which the genes of one parent are excluded from gametes in the offspring of one sex. Bull (1979Bull ( , 1983 therefore considered four different systems with two sexes in which offspring of one sex transmit only the genome inherited from one parent. His preliminary conclusion was that systems with males transmitting only the maternal genome are more stable compared to the other three systems, which lack recombination (and may thus go extinct) and/or which are more likely to revert to diploidy or to evolve towards thelytoky.…”

“…His preliminary conclusion was that systems with males transmitting only the maternal genome are more stable compared to the other three systems, which lack recombination (and may thus go extinct) and/or which are more likely to revert to diploidy or to evolve towards thelytoky. Bull (1979) also provided an argument why pseudo-arrhenotoky may be more rare than arrhenotoky. Because uniparental males increase the transmission of maternal genes at the expense of the would-be father, there is selection in the most extreme form of genes that when transmitted through sperm avoid this elimination.…”