No sex in fungus-farming ants or their crops

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Asexual copy imposes evolutionary handicaps on asexual species, rendering them at risk of extinction, as a result of asexual replica generates novel genotypes and purges deleterious mutations at lower charges than sexual replica. Here, we report the primary case of whole asexuality in ants, the fungus-growing ant Mycocepurus smithii, the place queens reproduce asexually but workers are sterile, which is doubly enigmatic since the clonal colonies of M. smithii also rely on clonal fungi for food. Degenerate female mating anatomy, in depth box and laboratory surveys, and DNA fingerprinting implicate whole asexuality on this well-liked ant species. Maternally inherited bacteria (e.g. Wolbachia, Cardinium) and the fungal cultivars can also be ruled out as brokers inducing asexuality. M. smithii societies of clonal women provide a novel device to check theories of guardian–offspring war and reproductive policing in social insects.

Asexuality of both ant farmer and fungal crop demanding situations traditional views proposing that sexual farmer ants outpace coevolving sexual crop pathogens, and thus atone for vulnerabilities in their asexual crops. Either the double asexuality of each farmer and crop may allow the host to completely exploit benefits of asexuality for unknown causes or widespread switching between plants (symbiont reassociation) generates novel ant–fungus mixtures, which would possibly compensate for any evolutionary handicaps of asexuality in M. smithii. Keywords: asexual, fungus-growing ants, symbiosis, Mycocepurus smithii, Wolbachia, thelytoky

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Six strains of evidence strengthen whole and endogenous asexuality in M. smithii: absence of males, vital degeneration of the female mating apparatus, DNA fingerprint identification between mothers and daughters, absence of sex-ratio-biasing endosymbiotic micro organism, and the lack to induce male production through antibiotic remedy or fungal substitution. M. smithii represents, to our knowledge, the primary case of a male-less species of ant, and the first case where women produce both reproductive and employee offspring by means of asexual means.

Degeneration of the female mating equipment renders cryptic intercourse not likely for M. smithii (Judson & Normark 1996; Normark et al. 2003) and could recommend that the evolutionary origin of M. smithii from a sexual ancestor may not be very contemporary. A extra far flung somewhat than recent foundation of asexuality is also consistent with the common Neotropical distribution of M. smithii from northern Argentina to northern Mexico. However, it’s imaginable the degeneration of the unused mating equipment could growth quickly. A coalescent research inside of a larger phylogenetic treatment of the Mycocepurus genus is had to infer the age of asexuality in M. smithii.

Asexuality in M. smithii could be brought about by way of an infection with endosymbionts equivalent to Wolbachia bacteria (Stouthamer et al. 1999), Cardinium bacteria (Zchori-Fein & Perlman 2004), undescribed microbes that can manipulate replica (Zchori-Fein & Perlman 2004), or through the fungal cultivar (Mueller 2002). Wolbachia has been discovered in numerous sexually reproducing ant species (Wenseleers et al. 1998) together with fungus-growing ants (Van Borm et al. 2003), but is absent in seven partially asexual ant species (Wenseleers & Billen 2000; Fournier et al. 2005; Pearcy et al. 2005). We file here that endosymbiotic microbes also appear to be absent within the asexual M. smithii.

While asexual reproduction of haploid men evolved from unfertilized eggs (arrhenotokous parthenogenesis) is a normal part of hymenopteran replica, asexual reproduction of diploid women folk from unfertilized eggs (thelytokous parthenogenesis) is exceedingly rare in ants. Only seven distantly similar ant species produce females asexually (Wenseleers & Billen 2000; Fournier et al. 2005; Pearcy et al. 2005; Ohkawara et al. 2006) essentially by means of unmated employees, starting from facultative asexual reproduction after queen death to nearly obligate asexuality during which the queen caste is absent or morphologically diminished (Itow et al. 1984; Schilder et al. 1999). However, males occur in all seven of those ant species, contrasting with the entire absence of males in M. smithii. Three distinct reproductive methods of asexuality therefore appear to exist in ants: (i) employee reproduction of ladies with a pattern towards queen loss (Messor capitatus, Platytherea punctata, Cerapachys biroi, Pristomyrmex pungens; Pearcy et al. 2005), (ii) a combined technique where mated queens produce staff sexually however new queens asexually (Cataglyphis cursor, Wasmannia auropunctata, Vollenhovia emeryi; Fournier et al. 2005; Pearcy et al. 2005; Ohkawara et al. 2006), and (iii) strict queen thelytoky with sterile staff (M. smithii). Pristomyrmex pungens used to be proposed as an obligate asexual since it reproduces by way of worker thelytoky; on the other hand, males with purposeful genitalia and standard spermatogenesis occur, indicating the potential for intercourse (Itow et al. 1984; Tsuji 1988). By contrast, M. smithii has advanced a novel technique through which queens produce both staff and new queens asexually, the place workers are utterly sterile (electronic supplementary subject material).

Theory predicts that long-term asexuality increases extinction possible as a result of absence of recombination constrains a species’ talent to conform, by way of producing novel genotypes and purging deleterious alleles at decrease charges, in the end rendering asexual lineages not as good as competing sexual lineages (Barton & Charlesworth 1998). This price of asexuality is also exacerbated in M. smithii thru its dependence on asexual cultivar propagation (Mueller et al. 1998, 2005). While cultivars of M. smithii aren’t historic asexuals (Mueller et al. 1998; Mueller 2002), they are cultivated clonally within a nest and between nests over a few years, making them liable to fungal pathogens evolving within the gardens (Currie et al. 2003). Dependence of an asexual host on an asexual symbiont may just due to this fact present a double value of asexuality. Alternatively, the asexuality of both ant and fungus would possibly allow the ants to completely exploit the evolutionary advantages of asexuality for unknown causes. In cyclic parthenogens comparable to Daphnia and aphids, asexual bureaucracy predominate all through useful resource abundance and turn to sexual reproduction when resources transform limiting (Williams 1975; Bell 1982; Lynch 1984). However, M. smithii confirmed no switch to sexuality throughout differences due to the season, environmental gradients, geographical vary (Argentina to Mexico), and numerous laboratory prerequisites studied to date.

Assuming a double asexuality handicap, it’s unclear how M. smithii could maintain one of the vital common distributions and biggest local abundances of all attine ant species (Rabeling 2004; Rabeling et al. 2007). Strict clonal reproduction may do away with kin-selected queen-worker conflicts that are thought to plague sexual insect societies (Ratnieks et al. 2006), and M. smithii due to this fact provides a novel experimental device to check theories of mother or father–offspring war and reproductive policing. In addition, not like all other fungus-growing ant species that typically specialize on a narrow clade of fungi, M. smithii is the only attine ant species recognized to domesticate a diversity of fungi between different nests. This unprecedented range of cultivars propagated within M. smithii arises because M. smithii continuously switches to novel, distantly comparable fungal vegetation (Mueller et al. 1998; A. G. Himler & U. G. Mueller 2004, unpublished information). Frequent switching between fungal crops (symbiont reassociation) may mitigate the double asexuality handicap as a result of switching generates novel combos of ant farmer and crop genomes. This potentially creates sufficient variation in synergistic ant–crop phenotypes to outpace coevolution by means of crop pathogens (Mueller 2002; Van Doninck et al. 2002) and cope with environmental fluctuations. One possibility is that M. smithii is a geographic parthenogen (Vandel 1928), i.e. it has a tendency to breed asexually in additional excessive altitudes, additional north, or extra extreme environments than their sexual family (Bell 1982; Lynch 1984). However, M. smithii has one of the vital in depth distributions of fungus-growing ants (Argentina to Mexico), and it is at all times sympatric with different, sexual attine species (aside from for some Caribbean island populations). Another possibility is that M. smithii can colonize a variety of habitats as it represents a ‘general purpose genotype’ (GPG) in a position to tolerate extensive environmental prerequisites (Lynch 1984), an evidence applied to the traditional asexual darwinulid ostracods (Van Doninck et al. 2002). If so, M. smithii will be the first case of a symbiosis GPG and beef up the recommendation that clonality leads in opposition to higher ecological generalization slightly than specialization.

The common distribution and ecological abundance of M. smithii problem traditional views proposing that sexuality allows fungus-growing ants to assume the coevolutionary arms races of their asexual cultivars (i.e. effectively converting crop–pathogen arms races into races between ant farmers and crop pathogens; Herre et al. 1999). Asexuality of M. smithii precludes the sort of hypothesized hands race switch, and the ecological luck of the twin asexual symbiosis between clonal ant farmers and their clonal crops therefore defies current theoretical expectancies, most likely including a singular type of asexual scandal if M. smithii is shown to be of extra ancient than contemporary evolutionary origin (Judson & Normark 1996; Normark et al. 2003). We are expecting that M. smithii will emerge not simplest as a new empirical device to test theories of father or mother–offspring war and policing in eusocial insects (Ratnieks et al. 2006), but additionally as a type permitting managed symbiont-switch experiments with a purpose to perceive the evolutionary endurance of asexual lineages inside of a community of coevolving sexual pathogens and asexual mutualists.

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