Cryptic recessive lethality of a supergene controlling social organization in ants

Abstract

Supergenes arise when structural changes (typically chromosomal inversions, but also deletions, duplications and repeat accumulations) or epigenetic changes suppress recombination between alternative haplotypes (Faria et al.,

A supergene controlling social structure in Alpine ants also affects the dispersal ability and fecundity of each sex

“…Lower fecundity of P males compared with M males and lower survival and fecundity of PP queens compared with MP or MM queens are probably caused by deleterious mutations that tend to accumulate in non-recombining genomic regions [ 26 , 60 , 61 ]. Recessive deleterious or lethal mutations have been reported in supergenes associated with diverse traits, such as social structure in ants [ 26 , 62 ], life-history traits in seaweed flies [ 63 ], mating morphs in ruffs [ 64 ] and white-throated sparrows [ 65 ], heterostyly in primroses [ 66 ] and taillessness in mice [ 67 ].…”

“…Lower fecundity of P males compared with M males and lower survival and fecundity of PP queens compared with MP or MM queens are probably caused by deleterious mutations that tend to accumulate in non-recombining genomic regions [ 26 , 60 , 61 ]. Recessive deleterious or lethal mutations have been reported in supergenes associated with diverse traits, such as social structure in ants [ 26 , 62 ], life-history traits in seaweed flies [ 63 ], mating morphs in ruffs [ 64 ] and white-throated sparrows [ 65 ], heterostyly in primroses [ 66 ] and taillessness in mice [ 67 ]. Deleterious mutations result from gene disruptions at inversion breakpoints, genetic drift due to small effective population size during early evolution of the inversion [ 68 ] and further accumulation of deleterious mutations by Muller’s ratchet [ 68 , 69 ] (although in rare cases, double crossovers and gene conversion can decrease these negative effects [ 70 , 71 ]).…”

“…This suggests that MP queens and MM queens mated to P males likely propagate the polygyne social form. Although in the wild over 70% of eggs laid in polygyne colonies have the PP genotype, PP workers suffer from very high mortality, as do PP queens in the laboratory, so that most surviving queens and workers in polygyne colonies have the MP genotype [ 26 ]. In addition, about 20% of MM queens mate with P males in swarms [ 29 ].…”

“…In both cases, the derived haplotype is dominant for polygyny, in the sense that females (queens and workers) carrying at least one copy of this haplotype establish polygyne colonies, while females lacking it establish monogyne colonies [19][20][21][22]. Moreover, in both lineages, the derived haplotype differs from the ancestral haplotype by several large inversions (which halts recombination between the two haplotypes) [23,24], has recessive deleterious effects [25,26] and displays selfish properties, albeit through different mechanisms [27,28]. Moreover, the two social supergenes are associated with alternative dispersal tactics and other correlated life-history traits.…”

“… Overview of the dispersal process of genetically determined social forms of F. selysi ( a ) and experiments carried out for each step of the dispersal process ( b ), with colours indicating the social supergene genotype of queens, males and workers, respectively ( c ). Effective gene flow between social forms, and the spread of each social form, depend on the number of colonies producing winged queens and males, and their sex allocation [ 29 , 32 , 37 ], the dispersal strategies of queens and males ([ 22 ] and experiments 1 and 2), the distance travelled before and after mating (experiments 1 and 2), the mating tactics of queens and males (experiment 3), the fecundity of queens and survival of their colonies ([ 26 , 38 , 39 ] and experiments 3 and 4) and the colony phenotype of each cross [ 19 , 22 ]. Different colours match each supergene genotype (blue: MM/M; orange: MP; red: PP/P ).…”