Abstract
The general prevalence of sexual reproduction over asexual reproduction among organisms testifies to the evolutionary benefits of recombination, such as accelerated adaptation to changing environments and elimination of deleterious mutations. Documented instances of asexual reproduction in groups otherwise dominated by sexual reproduction challenge evolutionary biologists to understand the special circumstances that might confer an advantage to asexual reproductive strategies. Here we report one such instance of asexual reproduction in the ants. We present evidence for obligate thelytoky in the asexual fungus-gardening ant, Mycocepurus smithii, in which queens produce female offspring from unfertilized eggs, workers are sterile, and males appear to be completely absent. Obligate thelytoky is implicated by reproductive physiology of queens, lack of males, absence of mating behavior, and natural history observations. An obligate thelytoky hypothesis is further supported by the absence of evidence indicating sexual reproduction or genetic recombination across the species' extensive distribution range (Mexico-Argentina). Potential conflicting evidence for sexual reproduction in this species derives from three Mycocepurus males reported in the literature, previously regarded as possible males of M. smithii. However, we show here that these specimens represent males of the congeneric species M. obsoletus, and not males of M. smithii. Mycocepurus smithii is unique among ants and among eusocial Hymenoptera, in that males seem to be completely absent and only queens (and not workers) produce diploid offspring via thelytoky. Because colonies consisting only of females can be propagated consecutively in the laboratory, M. smithii could be an adequate study organism a) to test hypotheses of the population-genetic advantages and disadvantages of asexual reproduction in a social organism and b) inform kin conflict theory.For a Portuguese translation of the abstract, please see S1.
Highlights
Explaining the prevalence of sexual over asexual reproduction has been a longstanding goal in evolutionary biology [1,2,3,4,5]
In order to test if thelytoky is widespread in queens of M. smithii and to investigate the behavioral ecological consequences of thelytoky in field populations, we studied the population biology, reproductive physiology of queens and workers, and the mating behavior of a M. smithii population in Brazil, and compared this population with two sexually reproducing, sympatric congeners
Mycocepurus smithii appears to be obligately asexual based on its reproductive physiology, and the absence of males and mating behavior
Summary
Explaining the prevalence of sexual over asexual reproduction has been a longstanding goal in evolutionary biology [1,2,3,4,5]. Over 20 models describing the advantages of sex have been proposed, differing with respect to the short- and long-term advantages of sexuality that outweigh its two-fold evolutionary cost [2,6,7,8]. The near absence of asexual lineages that persist over long evolutionary time suggests that the disadvantages of asexuality generally outweigh its benefits [13,14]. Asexuality is part of normal hymenopteran reproduction because males are produced via arrhenotoky (males develop from unfertilized, haploid eggs) [15,16]. Females develop from fertilized, diploid eggs [17,18]. Thelytokous parthenogenesis, the production of diploid female offspring from unfertilized eggs, has been observed in a small number of eusocial hymenopteran species. Thelytoky has been convincingly demonstrated in the Cape honeybee, Apis mellifera capensis [19,20,21], and for seven distantly related species of ants (see Discussion)
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