Ant queens cannibalise infected brood to contain disease spread and recycle nutrients

Filial cannibalism, where parents eat their own offspring, is a taxonomically widespread behaviour with a multitude of potential adaptive explanations. Of these, the impact of parasites on the expression of filial cannibalism is particularly poorly understood. On one hand, cannibalising young with low survival probability may enable parents to reinvest valuable resources into future reproduction; on the other, cannibalising offspring harbouring parasites that can potentially also infect the parents may select against this behaviour. Although disease-induced cannibalism of eggs has been reported in fish, the benefits of consuming infected brood to contain infections – as an explanation for the evolution of filial cannibalism – remains largely unexplored. Here, we demonstrate that solitarily founding ant queens cannibalise all sick larvae in their nests before they become contagious, showing clearly that filial cannibalism both (i) contains an otherwise lethal infection without any long-term consequences on queen survival and (ii) enables the reinvestment of recouped energy into additional egg production.


Ant queens cannibalise infected brood to contain disease spread and recycle nutrients
Flynn Bizzell 1 and Christopher D. Pull 1,2, * Filial cannibalism, where parents eat their own offspring, is a taxonomically widespread behaviour with a multitude of potential adaptive explanations 1 .Of these, the impact of pathogens on the expression of fi lial cannibalism is, in particular, poorly understood.Cannibalising young with low survival probability may enable parents to reinvest valuable resources into future reproduction 1 .However, cannibalising offspring that harbour pathogens may be potentially harmful to parents, and such risk may therefore select against this behaviour.Although disease-induced cannibalism of eggs has been reported in fi sh 2 , the benefi ts of consuming infected brood to contain infections -as an explanation for the evolution of fi lial cannibalism -remain largely unexplored.Here, we demonstrate that solitarily founding ant queens cannibalise sick larvae in their nests before they become contagious, showing that fi lial cannibalism both contains an otherwise lethal infection without any long-term consequences on queen survival and also enables the reinvestment of recouped energy into additional egg production.
Ant queens typically found colonies alone, and most such colonies fail due to predation, starvation, or infection of the queen or her brood by pathogens present in the microbially rich nest environment 3 .Although the collective disease defences performed by workers in mature social-insect colonies -termed social immunity -are well characterised 4 , we still know surprisingly little about the behavioural immunity of their founding individuals.Here, we report that founding queens of the black garden ant (Lasius niger) cannibalise their infected young and that this improves their chances of successful colony Correspondence foundation.Specifi cally, we exposed fi ve larvae per queen to infectious conidiospores of the fungal pathogen Metarhizium (strain isolated from a naturally infected L. niger founding queen).Larvae were left in isolation for 24 hours to develop lethal, but not yet transmissible, infections.As a control, larvae were exposed to a sham treatment and similarly isolated.All larvae were then returned to their nests and the queens' responses fi lmed.In total, we found that queens cannibalised 92% of infected larvae -leaving no remains -but only 6% of control larvae (Figure 1A and Video S1: likelihood ratio test (LR)-χ² = 89.23,df = 1, p < 0.0001; all sample sizes in fi gure legend).
To test if cannibalism is a response to infection or simply larval death, we presented queens with either uninfected control, infected, or freezekilled uninfected larvae.Although dead larvae were also cannibalised, infected larvae were consumed at substantially higher rates (Figure 1B: interaction between treatment and time, LRχ 2 = 65.09,df = 2, p < 0.0001; p  0.0003 for all post-hoc comparisons).Queens likely detect active infections through post-infection changes in larval cuticular hydrocarbons, which have been shown to trigger the elimination

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Current Biology 34, R837-R853, September 23, 2024 R849 ll of sick brood in both ant and honeybee workers 4,5 .Despite the potential risk of infection, most queens survived the solitary period and produced workers (Figure S1A), with no differences in fi nal colony size nor composition between treatments (Figure S1B).Ant queens may minimise their risk of contracting infections via cannibalism by swallowing their acidic, antimicrobial venom, which in workers creates a gut environment that neutralises pathogens 6 .Indeed, we anecdotally observed queens grooming the abdominal venom-gland opening.
To understand why queens consume their infected young, we simulated a failure to detect and cannibalise sick brood by presenting queens with larvae where the infection had progressed to the terminal stage (sporulation) or control larvae.Sporulation occurs once the fungus has consumed all host resources, leading to the production of fruiting bodies containing thousands of new, highly virulent infectious conidiospores 3 .Queens groomed and sprayed the sporulating cadavers with antimicrobial venom (Video S1) but despite these apparent attempts to contain the infection, 80% of queens contracted the disease and died in the infectious cadaver group (Figure 1C: infectious vs. control, LR-χ² = 20.3,df = 1, p < 0.0001; n = 15 queens in both treatments).Even when the queen did survive, her healthy brood were all lost to secondary infections.
Adaptive 'energy-benefi t' explanations for the evolution of fi lial cannibalism predict that parents should consume their brood under unfavourable conditions, so that recouped resources can be redirected into future reproduction 1 .We found that queens who cannibalised their infected larvae laid an additional 55% more eggs than non-cannibalising control queens (Figure 1D: t = -3.30,df = 26.45,p = 0.003; n = 15 infected and 18 controls).This higher rate of egg laying could be a compensatory strategy caused by exposure to infected brood.However, the reinvestment of recouped nutrients back into egg production is more likely and may be especially critical for founding queens, which do not forage and are therefore severely resource limited, surviving solely on the breakdown of bodily reserves 7 .Producing enough brood is essential as intraspecifi c competition with neighbouring nests is a major driver of incipient colony failure, and larger colonies invariably win 7 .
Combined, our results reveal that fi lial cannibalism by ant queens prevents brood infections that cause colony-founding failure.Given how readily ant queens perform 'hygienic cannibalism', it is surprising that worker ants in mature colonies do not express this behaviour.There are two potential explanations for this difference.First, unlike workers 8 , queens cannot readily dispose of infected brood by discarding them outside of the nest because they seal themselves into their claustral cell.Secondly, queens naturally require a high-protein diet to fuel egg production, whereas worker lifespan is shortened by consuming too much protein 9 .In contrast to ants, cannibalism of healthy, infected, and dead nestmates by termite workers is commonly observed 10 .Like founding ant queens, many termites live in 'closed' nests, precluding extranidal corpse disposal, and their high cellulose diet makes other nestmates a rare source of protein.Like the termites, we found that ant queens also cannibalise dead (freeze-killed) brood.Consequently, cannibalism solves the same problem of disease containment and corpse disposal in a confi ned space for both founding ant queens and termite colonies, whilst simultaneously ensuring valuable nutrients are not wasted.
In conclusion, our study reveals that preventing the spread of infections among brood, coupled with the benefi cial recovery of resources from sick offspring, is an adaptive benefi t of fi lial cannibalism -a previously predicted but hitherto untested hypothesis 2 .Additionally, we fi nd social insect queens are remarkably effective at responding to and eliminating earlystage infections before they become transmissible, a key tenant of disease defence in mature ant, bee, and termite colonies 4,5 .

Figure 1 .
Figure 1.Cannibalism of infected brood by ant queens.(A) Ant queens cannibalise more larvae infected with the fungal pathogen Metarhizium than sham-treated controls (n = 10 for both).Bars show proportion ± 95% confi dence intervals.(B) Infected larvae are cannibalised at faster rates compared with control or freeze-killed larvae (n = 26 control, 23 infected and 23 freeze-killed).Points represent the total proportion of larvae cannibalised per day, aggregated across all replicates within each treatment group.Logistic regression curves ± 95% confi dence intervals depict the predicted probability of cannibalism over time using the full data set, estimated by a generalised linear model with binomial errors.(C) Queen survival probability is drastically reduced when they fail to cannibalise infected larvae (n = 15 queens in both treatments).Crosshairs denote surviving queens.(D) Queens that cannibalise infected larvae subsequently lay more eggs than control queens that do not perform cannibalism (n = 15 infected and 18 controls).Error bars show mean ± 95% confi dence intervals and each point represents one replicate.(A-D) Letters denote signifi cantly different groups (p < 0.05).