The ecological success of a social parasite increases with manipulation of collective host behaviour

Many parasites alter the behaviour of their host to their own advantage, yet hosts often vary in their susceptibility to manipulation. The ecological and evolutionary implications of such variation can be profound, as resistant host populations may suffer lower parasite pressures than those susceptible to manipulation. To test this prediction, we assessed parasite‐induced aggressive behaviours across 16 populations of two Temnothorax ant species, many of which harbour the slavemaker ant Protomognathus americanus. This social parasite uses its Dufour's gland secretions to manipulate its hosts into attacking nestmates, which may deter defenders away from itself during invasion. We indeed find that colonies that were manipulated into attacking their Dufour‐treated nestmates were less aggressive towards the slavemaker than those that did not show slavemaker‐induced nestmate attack. Slavemakers benefited from altering their hosts’ aggression, as both the likelihood that slavemakers survived host encounters and slavemaker prevalence in ant communities increased with slavemaker‐induced nestmate attack. Finally, we show that Temnothorax longispinosus colonies were more susceptible to manipulation than Temnothorax curvispinosus colonies. This explains why T. curvispinosus colonies responded with more aggression towards invading slavemakers, why they were less likely to let slavemakers escape and why they were less frequently parasitized by the slavemaker than T. longispinosus. Our findings highlight that large‐scale geographic variation in resistance to manipulation can have important implications for the prevalence and host preference of parasites.     

TEMPORAL VARIATION FAVORS THE EVOLUTION OF GENERALISTS IN EXPERIMENTAL POPULATIONS OF DROSOPHILA MELANOGASTER

In variable environments, selection should favor generalists that maintain fitness across a range of conditions. However, costs of adaptation may generate fitness trade‐offs and lead to some compromise between specialization and generalization that maximizes fitness. Here, we evaluate the evolution of specialization and generalization in 20 populations of Drosophila melanogaster experimentally evolved in constant and variable thermal environments for 3 years. We developed genotypes from each population at two temperatures after which we measured fecundity across eight temperatures. We predicted that constant environments would select for thermal specialists and that variable environments would select for thermal generalists. Contrary to our predictions, specialists and generalists did not evolve in constant and spatially variable environments, respectively. However, temporal variation produced a type of generalist that has rarely been considered by theoretical models of developmental plasticity. Specifically, genotypes from the temporally variable selective environment were more fecund across all temperatures than were genotypes from other environments. These patterns suggest certain allelic effects and should inspire new directions for modeling adaptation to fluctuating environments.     

Constraints on adaptation of Escherichia coli to mixed‐resource environments increase over time

Can a population evolved in two resources reach the same fitness in both as specialist populations evolved in each of the individual resources? This question is central to theories of ecological specialization, the maintenance of genetic variation, and sympatric speciation, yet relatively few experiments have examined costs of generalism over long‐term adaptation. We tested whether selection in environments containing two resources limits a population's ability to adapt to the individual resources by comparing the fitness of replicate Escherichia coli populations evolved for 6000 generations in the presence of glucose or lactose alone (specialists), or in varying presentations of glucose and lactose together (generalists). We found that all populations had significant fitness increases in both resources, though the magnitude and rate of these increases differed. For the first 4000 generations, most generalist populations increased in fitness as quickly in the individual resources as the corresponding specialist populations. From 5000 generations, however, a widespread cost of adaptation affected all generalists, indicating a growing constraint on their abilities to adapt to two resources simultaneously. Our results indicate that costs of generalism are prevalent, but may influence evolutionary trajectories only after a period of cost‐free adaptation.     

Larval recognition by Temnothorax longispinosus and T. ambiguus hosts of the slave-making ant Protomognathus americanus revisited: colony-level referent ensures conspecific preference

Slave-making ants exploit the labour of their own or another species. Temnothorax ambiguus and T. longispinosus are both ant species that serve as hosts of the obligatory slave-making ant Protomognathus americanus and are facultative slave-makers themselves. We offered laboratory colonies of T. ambiguus and T. longispinosus a series of choices among different larval types to better understand their brood discrimination abilities. Workers of both species preferentially accepted nestmate over non-nestmate larvae. Both species preferentially retrieved unrelated conspecific larvae over congeneric allospecific larvae, and T. ambiguus workers consumed more allospecifics than conspecifics. When presented with conspecific versus P. americanus larvae, both species manifested a clear bias towards conspecific larvae in terms of earlier retrieval and reduced cannibalism. That workers did not prefer P. americanus larvae over conspecific larvae as documented in previous research likely reflects the fact that in the present study, subject workers had access to the entirety of their colony as a referent during rearing and at the time of testing, as they would in nature. Moreover, reciprocal contact between P. americanus and conspecific larvae increased acceptance of the slave-maker larvae, but did not appear to lessen the acceptability of conspecific larvae. This suggests that transfer of cues through contact may be sufficient to alter the recognition signature of P. americanus larvae increasing acceptability by their hosts.     

Geographic distribution of the anti-parasite trait “slave rebellion”

Social parasites exploit the brood care behavior of other species and can exert strong selection pressures on their hosts. As a consequence, hosts have developed defenses to circumvent or to lower the costs of parasitism. Recently, a novel, indirect defense trait, termed slave rebellion, has been described for hosts of a slave-making ant: Enslaved Temnothorax longispinosus workers reduce local parasite pressure by regularly killing pupae of their obligatory slavemaking parasite Protomognathus americanus. Subsequently, growth of social parasite nests is reduced, which leads to fewer raids and likely increases fitness of neighboring related host colonies. In this study, we investigate the presence and expression the slave rebellion trait in four communities. We report its presence in all parasitized communities, document strong variation in its expression between different geographic sites and discuss potential explanations for this observed variation.     

Evolutionary increases in defense during a biological invasion

Invasive plants generally escape from specialist herbivores of their native ranges but may experience serious damage from generalists. As a result, invasive plants may evolve increased resistance to generalists and tolerance to damage. To test these hypotheses, we carried out a common garden experiment comparing 15 invasive populations with 13 native populations of Chromolaena odorata, including putative source populations identified with molecular methods and binary choice feeding experiments using three generalist herbivores. Plants from invasive populations of C. odorata had both higher resistance to three generalists and higher tolerance to simulated herbivory (shoot removal) than plants from native populations. The higher resistance of plants from invasive populations was associated with higher leaf C content and densities of leaf trichomes and glandular scales, and lower leaf N and water contents. Growth costs were detected for tolerance but not for resistance, and plants from invasive populations of C. odorata showed lower growth costs of tolerance. Our results suggest that invasive plants may evolve to increase both resistance to generalists and tolerance to damage in introduced ranges, especially when the defense traits have low or no fitness costs. Greater defenses in invasive populations may facilitate invasion by C. odorata by reducing generalist impacts and increasing compensatory growth after damage has occurred.     

Towards greater realism in inclusive fitness models: the case of worker reproduction in insect societies

The conflicts over sex allocation and male production in insect societies have long served as an important test bed for Hamilton''s theory of inclusive fitness, but have for the most part been considered separately. Here, we develop new coevolutionary models to examine the interaction between these two conflicts and demonstrate that sex ratio and colony productivity costs of worker reproduction can lead to vastly different outcomes even in species that show no variation in their relatedness structure. Empirical data on worker-produced males in eight species of Melipona bees support the predictions from a model that takes into account the demographic details of colony growth and reproduction. Overall, these models contribute significantly to explaining behavioural variation that previous theories could not account for.     

Wingless virgin queens assume helper roles in Acromyrmex leaf-cutting ants

Division of labour is the hallmark of advanced societies, because specialization carries major efficiency benefits in spite of costs owing to reduced individual flexibility [1]. The trade-off between efficiency and flexibility is expressed throughout the social insects, where facultative social species have small colonies and reversible caste roles and advanced eusocial species have permanently fixed queen and worker castes. This usually implies that queens irreversibly specialize on reproductive tasks [2]. Here, we report an exception to this rule by showing that virgin queens (gynes) of the advanced eusocial leaf-cutting ant Acromyrmex echinatior switch to carrying out worker tasks such as brood care and colony defence when they fail to mate and disperse. These behaviours allow them to obtain indirect fitness benefits (through assisting the reproduction of their mother) after their direct fitness options (their own reproduction) have become moot. We hypothesize that this flexibility could (re-)evolve secondarily because these ants only feed on fungal mycelium and thus could not benefit from cannibalising redundant gynes, and because queens have retained behavioural repertoires for foraging, nursing, and defense, which they naturally express during colony founding.     

Genetic Resistance to Bacillus thuringiensis Alters Feeding Behaviour in the Cabbage Looper,Trichoplusia ni

Evolved resistance to xenobiotics and parasites is often associated with fitness costs when the selection pressure is absent. Resistance to the widely used microbial insecticide Bacillus thuringiensis (Bt) has evolved in several insect species through the modification of insect midgut binding sites for Bt toxins, and reports of costs associated with Bt resistance are common. Studies on the costs of Bt-resistance restrict the insect to a single artificial diet or host-plant. However, it is well documented that insects can self-select appropriate proportions of multiple nutritionally unbalanced foods to optimize life-history traits. Therefore, we examined whether Bt-resistant and susceptible cabbage loopers Trichoplusia ni differed in their nutrient intake and fitness costs when they were allowed to compose their own protein:carbohydrate diet. We found that Bt-resistant T. ni composed a higher ratio of protein to carbohydrate than susceptible T. ni. Bt-resistant males exhibited no fitness cost, while the fitness cost (reduced pupal weight) was present in resistant females. The absence of the fitness cost in resistant males was associated with increased carbohydrate consumption compared to females. We demonstrate a sex difference in a fitness cost and a new behavioural outcome associated with Bt resistance.     

Mechanisms of social regulation change across colony development in an ant

Background  

Mutual policing is an important mechanism for reducing conflict in cooperative groups. In societies of ants, bees, and wasps, mutual policing of worker reproduction can evolve when workers are more closely related to the queen's sons than to the sons of workers or when the costs of worker reproduction lower the inclusive fitness of workers. During colony growth, relatedness within the colony remains the same, but the costs of worker reproduction may change. The costs of worker reproduction are predicted to be greatest in incipient colonies. If the costs associated with worker reproduction outweigh the individual direct benefits to workers, policing mechanisms as found in larger colonies may be absent in incipient colonies.     

Local feeding specialization by badgers (Meles meles) in a mediterranean environment

A case of local feeding specialization in the European badger (Meles meles), a carnivore species with morphological, physiological and behavioural traits proper to a trophic generalist, is described. For the first time, we report a mammalian species, the European rabbit (Oryctolagus cuniculus), as the preferred prey of badgers. Secondary prey are consumed according to their availability, compensating for temporal fluctuations in the abundance of rabbit kittens. We discuss how both predator (little ability to hunt) and prey (profitability and predictability) features, may favour the observed specialization, as predicted by foraging theory. Badgers show a trend to specialize on different prey in different areas throughout the species range. It is suggested that changes in prey features can reverse the badger feeding strategy at the population level. Such dynamic behavioural responses make difficult to label badgers as generalists or specialists at the species level.     

Genetic effects on task performance,but not on age polyethism,in a swarm-founding eusocial wasp

Division of labour among workers in insect societies often includes two major components: age-related changes in behaviour (age polyethism) and specialization in task performance. The aim of this study was to test whether similarity in inside-nest task performance and in rate of age polyethism correspond to genetic similarity among nestmates in the polygynous eusocial waspPolybia aequatorialis.Behavioural data were collected on marked, known-age workers from three source colonies introduced into two observation colonies in the field. Genetic similarity among workers was assessed by quantifying sharing of random amplified polymorphic DNA (RAPD) marker alleles. Workers were categorized by whether they engaged in nest cleaning as an indicator of individual differences in inside-nest task performance. Within source colonies, workers that performed nest-cleaning tasks were more genetically similar to each other than they were to workers not performing these tasks. Workers also differed in their rates of passage through the age-related task sequence, but no association was found between sharing of RAPD marker alleles and rate of age polyethism. These results accord with earlier studies demonstrating flexibility in age polyethism in swarm-founding wasps, and with findings that worker genotypic variability corresponds to specialization in task performance inP. aequatorialis. Polybiaspp. workers rarely switch among tasks, even in response to changes in colony conditions, and workers’ genotypes may constrain flexibility in task performance at the individual level. Conversely, colonies may accrue benefits from having genotypically diverse worker forces, which could favour the maintenance of polygyny in swarm-founding wasps.     

Consistency pays: sex differences and fitness consequences of behavioural specialization in a wide-ranging seabird

Specialists and generalists often coexist within a single population, but the biological drivers of individual strategies are not fully resolved. When sexes differ in their foraging strategy, this can lead them to different environmental conditions and stability across their habitat range. As such, sexual segregation, combined with dominance, may lead to varying levels of specialization between the sexes. Here, we examine spatial and temporal niche width (intraindividual variability in aspects of foraging behaviour) of male and female black-browed albatrosses (Thalassarche melanophrys), and its consequences for fitness. We show that females, where maximum foraging range is under fluctuating selection, exhibit more variable behaviours and appear more generalist than males, who are under directional selection to forage close to the colony. However within each sex, successful birds had a much narrower niche width across most behaviours, suggesting some specialization is adaptive in both sexes. These results demonstrate that while there are sex differences in niche width, the fitness benefit of specialization in spatial distribution is strong in this wide-ranging seabird.     

Developmental plasticity in the queen-polymorphic ant Temnothorax longispinosus

Females of social Hymenoptera show developmental plasticity in response to varying social and environmental conditions, though some species have strong genetic influences on the form of the female reproductives. In ants, a queen polymorphism can occur in which large queens initiate new colonies on their own, while small queens enter established nests. Most queen polymorphisms studied to date originate due to genetic differences between individuals of differing form. Here, we report on the development of female form in response to social factors within the nest in the queen-polymorphic ant Temnothorax longispinosus. Three queen size morphs occur: a rare large queen with higher fat stores that can found new colonies independently, a large queen that has low fat stores and is behaviorally flexible, and a small queen that rejoins the natal nest. Both in nesting units collected from the field and those reared in the lab, queen presence during larval development led to fewer larvae developing as gynes (virgin, winged queens), and most of those gynes were the small morph. This queen effect is transferred to developing gyne larvae by close, physical interaction between queens and workers, and causes slower larval development. We conclude that gyne size, and therefore reproductive behavior, in T. longispinosus is developmentally plastic in response to queen presence. Plasticity in reproductive behavior may be an adaptive response to the nest sites utilized by this species. T. longispinosus nests predominantly in acorns and hickory nuts, which can vary dramatically from 1 year to the next. Since queens are more likely to be present in each nesting unit when fewer nest sites are available, the queen effect that results in more small gynes produced links the expression of colony-founding traits to ecological conditions across habitat patches.     

Testing an Adaptive Hypothesis Through Context-Dependence: Effects of Water Depth on Foraging Behaviour in Three Species of Garter Snakes

Adaptive hypotheses based on interspecific comparisons can be tested by evaluating the context‐dependence of the behaviour of individual organisms. Drummond (Behaviour, 86, 1983, 1) categorized garter snake species (Thamnophis) as terrestrial–aquatic generalists or aquatic specialists based on diet and aquatic foraging behaviour. He hypothesized that the characteristic foraging behaviours of aquatic specialists – including frequent crawling on the underwater substrate and a high rate of underwater predatory strikes – are adaptations for feeding on relatively widely dispersed aquatic prey. Drummond's hypothesis based on interspecific comparisons suggests that individual snakes might change their foraging in the direction of aquatic specialist behaviour with an increase in water depth (which increases prey dispersion). I tested this prediction through laboratory observations of Mexican Pacific lowlands garter snakes (T. validus) feeding on minnows in shallow (2 cm) and deep (3–7 cm) water. Members of this species are appropriate subjects because they are ecologically intermediate between the generalists and aquatic specialists studied by Drummond, and thus might be expected to show more variation in aquatic foraging behaviour than those species. T. validus showed significantly higher frequencies of crawling on the underwater substrate and of underwater strikes in the deep water than in the shallow water; i.e. increased water depth shifted the behaviour of these snakes toward that of aquatic specialists, thus supporting Drummond's hypothesis. Individuals of an aquatic specialist species, the narrow‐headed garter snake (T. rufipunctatus), showed less pronounced changes in behaviour with increased water depth. Western ribbon snakes (T. proximus), which feed primarily at the land–water interface (and are expected to act like terrestrial–aquatic generalists), typically refused to feed in deep water. Interspecific differences in underwater visual acuity may underly the behavioural differences among the three species by determining whether changes in foraging behaviour with water depth are advantageous. Information on phylogenetic relationships suggests that the facultative behaviour of T. validus may represent an intermediate stage in the evolution of aquatic specialization.     

Kinship,parental manipulation and evolutionary origins of eusociality

One of the hallmarks of eusociality is that workers forego their own reproduction to assist their mother in raising siblings. This seemingly altruistic behaviour may benefit workers if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If worker presence is advantageous to mothers, however, eusociality may evolve without net benefits to workers. Indirect fitness benefits are often cited as evidence for the importance of inclusive fitness in eusociality, but have rarely been measured in natural populations. We compared inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusociality is optional. Our results show that workers have significantly lower inclusive fitness than females that found their own nests. In mathematical simulations based on M. genalis field data, eusociality cannot evolve with reduced intra-nest relatedness. The simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when helping behaviour was simulated as the result of maternal manipulation, but not as worker altruism. Thus, eusociality in M. genalis is best explained through kin selection, but the underlying mechanism is likely maternal manipulation.     

Nestmate Recognition in Leptothoracine Ants: Testing Fielde's Progressive Odor Hypothesis

Fielde's progressive odor hypothesis postulates that certain hereditary nestmate recognition odors in adult ants change progressively with age such that workers will often not accept older siblings that differ from them in age by as little as 40–60 days unless they eclosed among siblings of that age class and learned their recognition cues. Fielde's hypothesis was based on extensive but unsystematic experimental studies which fail to provide unequivocal evidence for this phenomenon. The present study tested this hypothesis for three closely-related ant species, Leptothorax ambiguus, L. curvispinosus, and L. longispinosus, by introducing workers between groups with known age structures and a minimum age difference of eight months. The results invalidate Fielde's hypothesis for these ants. However, progressive odors may yet be found in other species and may be associated with age polyethism.     

Substantial direct fitness gains of workers in a highly eusocial ant

Hamilton's theory of inclusive fitness suggests that helpers in animal societies gain fitness indirectly by increasing the reproductive performance of a related beneficiary. Helpers in cooperatively breeding birds, mammals and primitively eusocial wasps may additionally obtain direct fitness through inheriting the nest or mating partner of the former reproductive. Here, we show that also workers of a highly eusocial ant may achieve considerable direct fitness by producing males in both queenless and queenright colonies. We investigated the reproductive success of workers of the ant Temnothorax crassispinus in nature and the laboratory by dissecting workers and determining the origin of males by microsatellite analysis. We show that workers are capable of activating their ovaries and successfully producing their sons independently of the presence of a queen. Genotypes revealed that at least one fifth of the males in natural queenright colonies were not offspring of the queen. Most worker‐produced males could be assigned to workers that were unrelated to the queen, suggesting egg‐laying by drifting workers.     

Individual Specialization to Non-Optimal Hosts in a Polyphagous Marine Invertebrate Herbivore

Factors determining the degree of dietary generalism versus specialism are central in ecology. Species that are generalists at the population level may in fact be composed of specialized individuals. The optimal diet theory assumes that individuals choose diets that maximize fitness, and individual specialization may occur if individuals'' ability to locate, recognize, and handle different food types differ. We investigate if individuals of the marine herbivorous slug Elysia viridis, which co-occur at different densities on several green macroalgal species in the field, are specialized to different algal hosts. Individual slugs were collected from three original algal host species (Cladophora sericea, Cladophora rupestris and Codium fragile) in the field, and short-term habitat choice and consumption, as well as long-term growth (proxy for fitness), on four algal diet species (the original algal host species and Chaetomorpha melagonium) were studied in laboratory experiments. Nutritional (protein, nitrogen, and carbon content) and morphological (dry weight, and cell/utricle volume) algal traits were also measured to investigate if they correlated with the growth value of the different algal diets. E. viridis individuals tended to choose and consume algal species that were similar to their original algal host. Long-term growth of E. viridis, however, was mostly independent of original algal host, as all individuals reached a larger size on the non-host C. melagonium. E. viridis growth was positively correlated to algal cell/utricle volume but not to any of the other measured algal traits. Because E. viridis feeds by piercing individual algal cells, the results indicate that slugs may receive more cytoplasm, and thus more energy per unit time, on algal species with large cells/utricles. We conclude that E. viridis individuals are specialized on different hosts, but host choice in natural E. viridis populations is not determined by the energetic value of seaweed diets as predicted by the ODT.