Persistence of the single lineage of transmissible ‘social cancer’ in an asexual ant

Abstract

How cooperation can arise and persist, given the threat of cheating phenotypes, is a central problem in evolutionary biology, but the actual significance of cheating in natural populations is still poorly understood. Theories of social evolution predict that cheater lineages are evolutionarily short-lived. However, an exception comes from obligate socially parasitic species, some of which thought to have arisen as cheaters within cooperator colonies and then diverged through sympatric speciation. This process requires the cheater lineage to persist by avoiding rapid extinction that would result from the fact that the cheaters inflict fitness cost on their host. We examined whether this prerequisite is fulfilled, by estimating the persistence time of cheaters in a field population of the parthenogenetic ant Pristomyrmex punctatus. Population genetic analysis found that the cheaters belong to one monophyletic lineage which we infer has persisted for 200-9200 generations. We show that the cheaters migrate and are thus horizontally transmitted between colonies, a trait allowing the lineage to avoid rapid extinction with its host colony. Although horizontal transmission of disruptive cheaters has the potential to induce extinction of the entire population, such collapse is likely averted when there is spatially restricted migration in a structured population, a scenario that matches the observed isolation by distance pattern that we found. We compare our result with other examples of disruptive and horizontally transmissible cheater lineages in nature.

Public goods dilemma in asexual ant societies

“…Studies of experimental evolution using microbial cooperative systems have demonstrated the importance of high relatedness in their evolution (22,49). In P. punctatus, our previous population genetics study showed that the rate of worker migration among colonies in the study population was very low, at ∼10 −5 per generation (40). The restriction of migration is likely explained by the operation of a nestmate discrimination system [although condition-dependent to some extent (51-54)].…”

“…Our previous study indicated that cheaters had a much higher migration rate among colonies than cooperators, estimated at 10 −2 per generation (40). Therefore, cheaters can avert the immediate extinction of their own lineage by acting like a "transmissible social cancer" (40,58). The differential migration rates might be explained by the adaptation of the cheaters during the time they adaptation.…”

“…Reproductive division of labor is realized through age polyethism (or temporal castes) among workers, where younger workers reproduce and engage in inside-nest tasks, such as brood care, and older workers cease reproduction and shift to outside-nest tasks, such as foraging (38). Cheater individuals, which constitute a single intraspecific lineage in the field (39,40), engage in few tasks except for reproduction (41). In addition, these individuals show several characteristics that are typical in queens of other ants, such as having more ovarioles, a larger body size, and three conspicuous ocelli (39)(40)(41)(42).…”

“…Cheater individuals, which constitute a single intraspecific lineage in the field (39,40), engage in few tasks except for reproduction (41). In addition, these individuals show several characteristics that are typical in queens of other ants, such as having more ovarioles, a larger body size, and three conspicuous ocelli (39)(40)(41)(42). Using experimental colonies with varying proportions of cheaters, we tested whether the fitness of cheaters and workers in a colony of P. punctatus conformed to the framework of the public goods dilemma.…”

Genetic reincarnation of workers as queens in the Eastern honeybee Apis cerana

“…Thelytoky has already led to the evolution of specialised social parasites as in the Cape honeybee A. m. capensis (Goudie and Oldroyd, 2014) and the ant Pristomyrmex punctatus (Dobata et al, 2009;Dobata et al, 2011). In the Cape honeybee the consequences of the parasitic lineage are devastating.…”