Solitary foundation or colony fission in ants: an intraspecific study shows that worker presence and number increase colony foundation success.

Dispersal and establishment strategies are highly variable. Each strategy is associated with specific costs and benefits, and understanding which factors favour or disfavour a strategy is a key issue in ecology and evolution. Ants exhibit several strategies of establishment, i.e. of colony foundation. Some species rely on winged queens that found new colonies alone when others found with accompanying workers (colony fission). The benefits conferred by these workers have been little studied and quantified, because comparing the costs and benefits of solitary foundation vs. colony fission is difficult when comparing different species. We investigated this using the ant Myrmecina graminicola, one of the few species that use both strategies. Young mated queens were allowed to found new colonies in the laboratory, with either zero (solitarily), two or four workers (colony fission). The presence of workers increased both survival and growth of the foundations over the first year, with more workers yielding higher growth. Few workers (as little as two workers) were sufficient to provide benefits, suggesting that in M. graminicola the strategy of colony fission may not dramatically decrease the number of new colonies produced compared to solitary foundation. Because queens performing solitary foundation or colony fission differ in dispersal (by flight vs. on foot), our results support the hypothesis that these two strategies of foundation coexist along a competition-colonization trade-off, where solitary foundation offers a colonization advantage, while colony fission has a competitive advantage.

Experimental evidence that increased surface temperature affects bioturbation by ants.

Ants are important bioturbators that actively produce biopores and move soil particles. They could be particularly affected by global warming as they are ectotherms. Nevertheless, they can indirectly regulate their temperature, through changes in their circadian cycles and the architecture of their nests (e.g. digging deep nests or using insulating materials). Nest architecture has been considered an expanded functional trait of ant colonies and thus sensitive to environmental changes such as increasing temperatures. This work aimed to study the nest architecture of ants as a functional trait and its effects on soil bioturbation. We hypothesized that, when exposed to increased surface temperatures, ants would increase their excavation activities, build deeper nests and alter the layout of chambers to maintain their preferred temperature and humidity, thus enhancing soil porosity. We allowed 17 young Lasius niger ant colonies to excavate nests in soil columns exposed to three surface temperatures (mild, n = 5; medium, n = 6; and high, n = 6) for 100 days. We measured the amount of soil excavated weekly and took X-ray scans of the soil column on Days 7, 14, 28, and 88 to characterize the three-dimensional structure of the nests (depth, shape, volume of chambers and tunnels). We then collected the colonies and measured their growth during the experiment, and the size and weight of workers. Ants reacted to surface temperature. Colonies exposed to medium and high temperatures excavated larger and deeper nests than those exposed to mild temperature. Nests excavated under high and medium temperatures had the same maximal depth, but chambers were located deeper in the former, which were further characterized by the refiling of some of the upper chambers. Colonies grew well in all treatments, although less under mild temperature. They produced normal-sized workers despite differences in surface temperature. Overall, these results suggest that ants exposed to higher temperatures live in deeper chambers. This study shows that surface temperature affects ant nest architecture, confirming its status as extended phenotype and highlighting its flexibility over time, which has in turn consequences on soil porosity.

No coordination required for resources allocation during colony fission in a social insect? An individual-based model reproduces empirical patterns.

Social insects are classic examples of cooperation and coordination. For instance, laboratory studies of colony relocation, or house-hunting, have investigated how workers coordinate their efforts to swiftly move the colony to the best nesting site available while preserving colony integrity, i.e. avoiding a split. However, several studies have shown that, in some other contexts, individuals may use private rather than social information and may act solitarily rather than in a coordinated way. Here, we study resource allocation by a mature ant colony when it reproduces by fissioning into several colonies. This is a very different task than house hunting in that colony fission seeks the split of the colony. We develop a simple individual-based model to test if colony fission and resource allocation may be carried out by workers acting solitarily with no coordination. Our model reproduces well the pattern of allocation observed in nature (number and size of new colonies). This does not show that workers do not communicate nor coordinate. Rather, it suggests that independent decision making may be an important component of the process of resource allocation.

To have and not to have sex: When multiple evolutions of conditional use of sex elegantly solve the question in the ant genus Cataglyphis.

Organisms use an amazingly large diversity of mechanisms to pass on their genes to the next generation. Sex is ancestral in eukaryotes, where it remains the most widespread way of reproduction. By combining one's genes with those of a partner, sex entails a dilution of one's genes at each generation. Evolution has been particularly creative in devising mechanisms allowing females to avoid this dilution, from classical parthenogenesis to the elimination of male genes after fertilization (Bell, 1982). Moreover, the term parthenogenesis includes various forms. Parthenogenesis can be used for female (thelytoky) or male (arrhenotoky) production and it can be associated with different cytological mechanisms, from strict clonality to meiotic division with the fusion of two of the four products of meiosis to restore diploidy (Suomalainen, Saura, & Lokki, 1987). Understanding the evolution of these diverse reproductive systems remains one of the most exciting and longstanding questions in evolutionary biology. By characterizing the reproductive systems of 11 species from the thermophilic ant genus Cataglyphis, in this issue of Molecular Ecology, Kuhn, Darras, Paknia, and Aron (2020) show the high lability of parthenogenesis, with multiple independent evolution of facultative thelytoky from sexual ancestors. The diversity of life history traits and social characteristics of this genus (e.g., mode of colony foundation, female polyandry) provides a unique and exciting opportunity to investigate the social and environmental factors driving the evolution of reproductive systems in social Hymenoptera.

Chemical Characterization of Young Virgin Queens and Mated Egg-Laying Queens in the Ant Cataglyphis cursor: Random Forest Classification Analysis for Multivariate Datasets.

Social insects are well known for their extremely rich chemical communication, yet their sex pheromones remain poorly studied. In the thermophilic and thelytokous ant, Cataglyphis cursor, we analyzed the cuticular hydrocarbon profiles and Dufour's gland contents of queens of different age and reproductive status (sexually immature gynes, sexually mature gynes, mated and egg-laying queens) and of workers. Random forest classification analyses showed that the four groups of individuals were well separated for both chemical sources, except mature gynes that clustered with queens for cuticular hydrocarbons and with immature gynes for Dufour's gland secretions. Analyses carried out with two groups of females only allowed identification of candidate chemicals for queen signal and for sexual attractant. In particular, gynes produced more undecane in the Dufour's gland. This chemical is both the sex pheromone and the alarm pheromone of the ant Formica lugubris. It may therefore act as sex pheromone in C. cursor, and/or be involved in the restoration of monogyny that occurs rapidly following colony fission. Indeed, new colonies often start with several gynes and all but one are rapidly culled by workers, and this process likely involves chemical signals between gynes and workers. These findings open novel opportunities for experimental studies of inclusive mate choice and queen choice in C. cursor.

Social Life in Arid Environments: The Case Study of Cataglyphis Ants.

Unlike most desert-dwelling animals, Cataglyphis ants do not attempt to escape the heat; rather, they apply their impressive heat tolerance to avoid competitors and predators. This thermally defined niche has promoted a range of adaptations both at the individual and colony levels. We have also recently discovered that within the genus Cataglyphis there are incredibly diverse social systems, modes of reproduction, and dispersal, prompting the tantalizing question of whether social diversity may also be a consequence of the harsh environment within which we find these charismatic ants. Here we review recent advances regarding the physiological, behavioral, life-history, colony, and ecological characteristics of Cataglyphis and consider perspectives on future research that will build our understanding of organic adaptive responses to desertification.

Strategies of offspring investment and dispersal in a spatially structured environment: a theoretical study using ants.

BACKGROUND: Offspring investment strategies vary markedly between and within taxa, and much of this variation is thought to stem from the trade-off between offspring size and number. While producing larger offspring can increase their competitive ability, this often comes at a cost to their colonization ability. This competition-colonization trade-off (CCTO) is thought to be an important mechanism supporting coexistence of alternative strategies in a wide range of taxa. However, the relative importance of an alternative and possibly synergistic mechanism-spatial structuring of the environment-remains the topic of some debate. In this study, we explore the influence of these mechanisms on metacommunity structure using an agent-based model built around variable life-history traits. Our model combines explicit resource competition and spatial dynamics, allowing us to tease-apart the influence of, and explore the interaction between, the CCTO and the spatial structure of the environment. We test our model using two reproductive strategies which represent extremes of the CCTO and are common in ants. RESULTS: Our simulations show that colonisers outperform competitors in environments subject to higher temporal and spatial heterogeneity and are favoured when agents mature late and invest heavily in reproduction, whereas competitors dominate in low-disturbance, high resource environments and when maintenance costs are low. Varying life-history parameters has a marked influence on coexistence conditions and yields evolutionary stable strategies for both modes of reproduction. Nonetheless, we show that these strategies can coexist over a wide range of life-history and environmental parameter values, and that coexistence can in most cases be explained by a CCTO. By explicitly considering space, we are also able to demonstrate the importance of the interaction between dispersal and landscape structure. CONCLUSIONS: The CCTO permits species employing different reproductive strategies to coexist over a wide range of life-history and environmental parameters, and is likely to be an important factor in structuring ant communities. Our consideration of space highlights the importance of dispersal, which can limit the success of low-dispersers through kin competition, and enhance coexistence conditions for different strategies in spatially structured environments.

Phenotypic plasticity and modularity allow for the production of novel mosaic phenotypes in ants.

BACKGROUND: The origin of discrete novelties remains unclear. Some authors suggest that qualitative phenotypic changes may result from the reorganization of preexisting phenotypic traits during development (i.e., developmental recombination) following genetic or environmental changes. Because ants combine high modularity with extreme phenotypic plasticity (queen and worker castes), their diversified castes could have evolved by developmental recombination. We performed a quantitative morphometric study to investigate the developmental origins of novel phenotypes in the ant Mystrium rogeri, which occasionally produces anomalous 'intercastes.' Our analysis compared the variation of six morphological modules with body size using a large sample of intercastes. RESULTS: We confirmed that intercastes are conspicuous mosaics that recombine queen and worker modules. In addition, we found that many other individuals traditionally classified as workers or queens also exhibit some level of mosaicism. The six modules had distinct profiles of variation suggesting that each module responds differentially to factors that control body size and polyphenism. Mosaicism appears to result from each module responding differently yet in an ordered and predictable manner to intermediate levels of inducing factors that control polyphenism. The order of module response determines which mosaic combinations are produced. CONCLUSIONS: Because the frequency of mosaics and their canalization around a particular phenotype may evolve by selection on standing genetic variation that affects the plastic response (i.e., genetic accommodation), developmental recombination is likely to play an important role in the evolution of novel castes in ants. Indeed, we found that most mosaics have queen-like head and gaster but a worker-like thorax congruent with the morphology of ergatoid queens and soldiers, respectively. Ergatoid queens of M. oberthueri, a sister species of M. rogeri, could have evolved from intercastes produced ancestrally through such a process.

Recurrent evolution of dependent colony foundation across eusocial insects.

The spectacular success of eusocial insects can be attributed to their sophisticated cooperation, yet cooperation is conspicuously absent during colony foundation when queens are alone. Selection against this solitary stage has led to a dramatically different strategy in thousands of eusocial insect species in which colonies are started by groups of nestmates and the benefits of sociality are retained continuously. Dependent colony foundation (DCF) evolved recurrently multiple times across the ants, bees, and wasps, though its prevalence in termites remains unclear. We review adaptations at both the colony level (reproductive investment shifts from sexuals to workers) and the individual level (wingless queens evolve in ants), and other consequences for life history (invasiveness, parasite transmission). Although few studies have focused on DCF, the accumulated data from anecdotal reports, supported by indirect information including morphology, population genetics, and colony demographics, make it clear that this strategy is more diverse and widespread than is usually recognized.

The influence of intraspecific competition on resource allocation during dependent colony foundation in a social insect.

Organisms face a trade-off between investment in fewer, larger offspring, or more, smaller offspring. Most organisms can adjust investment through variation in the size and number of offspring in response to factors such as resource availability and competition. In some social animals, established colonies divide into groups of individuals that become autonomous, a process known as colony fission (also dependent colony foundation in social insects). Resource allocation under fission can be fine-tuned by adjusting the number of new groups (offspring number) and the number of individuals in each new group (offspring size). We assessed the influence of competition on resource allocation during fission in the ant Cataglyphis cursor, by allowing colonies to fission in experimental enclosures of high or low conspecific colony density. The pattern of colony fission was similar to that observed in the field: each fissioning colony produced a few new nests comprising a highly variable number of workers and a single queen, the old queen was often replaced, and new queens were produced in excess. The number of new nests produced depended on the available workforce in the parent colony but was not affected by differences in colony density. Comparison with data from fission under natural field conditions, however, indicates that colonies in enclosures produced fewer, larger new nests, suggesting that resource investment patterns during fission are indeed subject to extrinsic factors. The density of conspecific colonies in the immediate surroundings may be an unreliable estimate of competition intensity and other factors should be considered.

Unequal resource allocation among colonies produced by fission in the ant Cataglyphis cursor.

How organisms allocate limited resources to reproduction is critical to their fitness. The size and number of offspring produced have been the focus of many studies. Offspring size affects survival and growth and determines offspring number in the many species where there is a trade-off between size and number. Many social insects reproduce by colony fission, whereby young queens and accompanying workers split off from a colony to form new colonies. The size of a new colony (number of workers) is set at the time of the split, and this may allow fine tuning size to local conditions. Despite the prevalence of colony fission and the ecological importance of social insects, little is known of colony fission except in honey bees. We studied colony fission in the ant Cataglyphis cursor. For clarity, "colony" and "nest" refer to colonies before and after colony fission, respectively (i.e., each colony fissions into several nests). The reproductive effort of colonies was highly variable: Colonies that fissioned varied markedly in size, and many colonies that did not fission were as large as some of the fissioning colonies. The mother queen was replaced in half of the fissioning colonies, which produced 4.0 +/- 1.3 (mean +/- SD) nests of markedly varied size. Larger fissioning colonies produced larger nests but did not produce more nests, and resource allocation among nests was highly biased. When a colony produced several nests and the mother queen was not replaced, the nest containing the mother queen was larger than nests with a young queen. These results show that the pattern of resource allocation differs between C. cursor and honey bees. They also suggest that C. cursor may follow a bet-hedging strategy with regard to both the colony size at which fission occurs and the partitioning of resources among nests. In addition, colony fission may be influenced by the age and/or condition of the mother queen, and the fact that workers allocating resources among nests have incomplete knowledge of the size and number of nests produced. These results show that the process of colony fission is more diverse than currently acknowledged and that studies of additional species are needed.

Variation in patriline reproductive success during queen production in orphaned colonies of the thelytokous ant Cataglyphis cursor.

In genetically diverse insect societies (polygynous or polyandrous queens), the production of new queens can set the ground for competition among lineages. This competition can be very intense when workers can reproduce using thelytoky as worker lineages that manage to produce new queens gain a huge benefit. Selection at the individual level might then lead to the evolution of cheating genotypes, i.e. genotypes that reproduce more than their fair share. We studied the variation in reproductive success among worker patrilines in the thelytokous and highly polyandrous ant Cataglyphis cursor. Workers produce new queens by thelytoky in orphaned colonies. The reproductive success of each patriline was assessed in 13 orphaned colonies using genetic analysis of 433 workers and 326 worker-produced queens. Our results show that patrilines contributed unequally to queen production in half of the colonies, and the success of patrilines was function of their frequencies in workers. However, over all colonies, we observed a significant difference in the distribution of patrilines between workers and worker-produced queens, and this difference was significant in three of 13 colonies. In addition, six colonies contained a low percentage of foreign workers (drifters), and in one colony, they produced a disproportionably high number of queens. Hence, we found some evidence for the occurrence of rare cheating genotypes. Nevertheless, cheating appears to be less pronounced than in the Cape Honey bee, a species with a similar reproductive system. We argue that worker reproduction by parthenogenesis might not be common in natural populations of C. cursor.

Self-sacrifice in 'desperado' contests between relatives.

Intra-specific competition occurs in all animal species and can lead to escalated conflict. Overt fighting entails the risk of injury or death, and is usually avoided through the use of conventions or pre-fight assessments. However, overt fighting can be expected when value of the contest outweighs the value of the future, as contestants have little or nothing to lose. In these situations, respect for conventions and asymmetries between contestants can break down, and overt fighting becomes more likely (the desperado effect). Such conditions can arise in contests between queens over colony ownership in social insects, because the value of inheriting a colony of potentially thousands of helpers is huge and queens may have very limited alternative reproductive options. However, in social species the balance of possible outcomes may be influenced by inclusive fitness, as contestants are often relatives. Here we present a simple model based on social insects, which demonstrates that not fighting can be selectively advantageous when there is a risk posed by fighting to inclusive fitness, even when not fighting is likely to result in death. If contestants are related, a loser can still gain indirect fitness through the winner, whereas fighting introduces a risk that both queens will die and thereby obtain zero inclusive fitness. When relatedness is high and fighting poses a risk of all contestants dying, it can be advantageous to cede the contest and be killed, rather than risk everything by fighting.

Bourgeois queens and high stakes games in the ant Aphaenogaster senilis.

BACKGROUND: Many animals face some form of conflict over reproductive opportunities. Queen selection in social insect colonies represents a high-stakes conflict where competition occurs among multiple queens for a few or a single reproductive role(s). The outcome of the contest is critical to the fitness of all colony individuals as most are sterile, and thus represents a conflict at multiple levels. Aphaenogaster senilis is a monogynous, monandrous, fission performing ant, in which queen selection occurs during colony fission and when replacement queens are produced to overcome orphaning. First-born queens are usually behaviourally dominant over subsequent queens, and eventually inherit the colony. We investigated the importance of physical dominance in queen selection in orphaned groups by manipulating the fighting ability of first-born queens via mandibular ablation. RESULTS: First emerged queens were heavier than second emerged queens, performed almost all aggression, were behaviourally dominant 92% of the time, and prevailed in 76% of groups after co-existing for 16 days on average. Mandibular ablation had no effect on queen behaviour or contest outcome. CONCLUSION: Aggression is probably ritualised and contests are decided by workers based on relative queen fertility. First-born queens thus have an inherent advantage over second-born queens as they have more time to develop ovaries. Subordinates never retaliated against aggression from dominants and this lack of retaliation can be interpreted as a form of bourgeois strategy as dominants were almost always first-born. However, the lack of alternative reproductive options makes not-fighting effectively a form of suicide. High relatedness between full-sister queens means that subordinates may be better off sacrificing themselves than risking injury to both queens by fighting.

No actual conflict over colony inheritance despite high potential conflict in the social wasp Polistes dominulus.

Social insect societies are outstanding examples of cooperation and conflict. Individuals work together, yet seek to increase their inclusive fitness at each others' expense. One such conflict is over colony inheritance, when a queen inherits the colony following the death of the previous queen. Colony inheritance is common in the social wasp Polistes dominulus, and it can have dramatic fitness consequences. The subordinate inheriting the colony is often unrelated to the initial foundress (alpha) and the workers, who therefore get zero inclusive fitness. Workers are capable of mating and reproducing, so that inheritance by a subordinate rather than by a related worker is surprising. Using patterns of egg-laying and egg destruction, we show in 32 laboratory colonies that, upon the removal of alpha, workers fully accepted a subordinate as the new breeder. This new alpha monopolized reproduction to the same extent as alpha, and there was no increase in reproduction by workers and other subordinates. Why workers accept a potentially unrelated subordinate as breeder rather than a full-sister worker is unclear. They may be constrained to do so, and they may seek fitness benefits by producing males later in the season or by absconding the nest.

How many gamergates is an ant queen worth?

Ant reproductives exhibit different morphological adaptations linked to dispersal and fertility. By reviewing the literature on taxa where workers can reproduce sexually (i.e. become gamergates) we show that (1) species with a single gamergate generally have lost the winged queen caste, whereas only half of the species with several gamergates have, and (2) single-gamergate species have smaller colonies than multiple-gamergate species. Comparison with "classical" ants without gamergates, where having one vs having several winged queens are two distinct syndromes, suggests that having one vs having several gamergates are not. Gamergate number does not affect the success of colony fission, but retention of the queen caste permits the option of independent foundation.

Direct assessment of queen quality and lack of worker suppression in a paper wasp.

Assessing a conspecific's potential is often crucial to increase one's fitness, e.g. in female choice, contests with rivals or reproductive conflicts in animal societies. In the latter, helpers benefit from accurately assessing the fertility of the breeder as an indication of inclusive fitness. There is evidence that this can be achieved using chemical correlates of reproductive activity. Here, we show that queen quality can be assessed by directly monitoring her reproductive output. In the paper wasp Polistes dominulus, we mimicked a decrease in queen fertility by regularly removing brood. This triggered ovarian development and egg-laying by many workers, which strongly suggests that brood abundance is a reliable cue of queen quality. Brood abundance can be monitored when workers perform regular brood care in small size societies where each brood element is kept in a separate cell. Our results also show that although the queen was not manipulated, and thus remained healthy and fully fertile, she did not control worker egg-laying. Nevertheless, when workers laid eggs, the queen secured a near reproductive monopoly by selectively destroying these eggs, a mechanism known as 'queen policing'. By contrast, workers destroyed comparatively few queen-laid eggs, but did destroy each other's eggs.

Pretender punishment induced by chemical signalling in a queenless ant.

Animal societies are stages for both conflict and cooperation. Reproduction is often monopolized by one or a few individuals who behave aggressively to prevent subordinates from reproducing (for example, naked mole-rats, wasps and ants). Here we report an unusual mechanism by which the dominant individual maintains reproductive control. In the queenless ant Dinoponera quadriceps, only the alpha female reproduces. If the alpha is challenged by another female she chemically marks the pretender who is then punished by low-ranking females. This cooperation between alpha and low-rankers allows the alpha to inflict punishment indirectly, thereby maintaining her reproductive primacy without having to fight.