[Show abstract][Hide abstract] ABSTRACT: One of the key features of eusociality is the seemingly altruistic behavior of workers who forego their own reproduction to assist their mother in raising siblings. This behavior may be adaptive if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If the presence of workers is sufficiently advantageous to mothers, however, worker fitness may not be the primary driver of eusocial evolution. This distinction is important, because indirect fitness benefits are often cited as prima facie evidence for the importance of kin selection in eusociality, but suitably large indirect fitness gains have rarely been demonstrated in natural populations. Here we compare the inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusocial nesting is optional. We show that inclusive fitness is similar among reproductive females with and without workers, but workers in eusocial nests have significantly lower inclusive fitness than would have been expected if they departed to found their own nests. In support for the role of kin selection in eusocial evolution, mathematical simulations based on M. genalis field data found eusociality cannot evolve with reduced intra-nest relatedness. In addition, the simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when simulated as a maternal trait (i.e., manipulation), but not when helping behavior was coded as a worker trait (i.e., altruism). Thus, eusociality in M. genalis is best explained through kin selection, but the mechanism being selected is likely maternal manipulation.
Entomological Society of America Annual Meeting 2014; 11/2014
[Show abstract][Hide abstract] ABSTRACT: Fungal symbionts that colonize leaf tissue asymptomatically (endophytes) can alter the foraging behaviour of leaf-cutting ants, and decrease the productivity of this herbivore's mutualistic fungal cultivar, Leucocoprinus gongylophorus. This negative effect of endophytes on the ant's cultivar could be the result of direct fungal–fungal interaction or indirect reductions in the quality of leaves, the cultivar's growth substratum. To test for the indirect effects, we measured in vitro growth rates of cultivars in media that contained sterilized leaf extracts from plants with high (Ehigh) and low (Elow) endophyte colonization. We found that, opposite to our expectations, cultivars grew significantly faster in Ehigh leaf extracts compared to Elow extracts. Our results suggest that endophyte-driven changes in leaf chemistry are a less likely explanation for the observed in vivo reduction in the ant's symbiotic fungal growth and imply that the effect of direct endophyte–cultivar interactions inside nests are potentially more important.
[Show abstract][Hide abstract] ABSTRACT: Social transmission and host developmental stage are thought to profoundly affect the structure of bacterial communities associated with honey bees and bumble bees, but these ideas have not been explored in other bee species. The halictid bees Megalopta centralis and Megalopta genalis exhibit intra-population social polymorphism, which we exploit to test whether bacterial communities differ by host social structure, developmental stage, or host species. We collected social and solitary Megalopta nests, and sampled bees and nest contents from all stages of host development. To survey these bacterial communities, we used 16S rRNA gene 454 pyrosequencing. We found no effect of social structure, but found differences by host species and developmental stage. Wolbachia prevalence differed between the two host species. Bacterial communities associated with different developmental stages appeared to be driven by environmentally acquired bacteria. A Lactobacillus kunkeei clade bacterium that is consistently associated with other bee species was dominant in pollen provisions and larval samples, but less abundant in mature larvae and pupae. Foraging adults appeared to often reacquire L. kunkeei clade bacteria, likely while foraging at flowers. Environmental transmission appears to be more important than social transmission for Megalopta bees at the cusp between social and solitary behavior. This article is protected by copyright. All rights reserved.
[Show abstract][Hide abstract] ABSTRACT: Ant social parasites evolve adaptive relationships with their hosts. Theoretically, coevolution predicts strong selection to maximize fitness of the parasite that minimizes costs to its host, which potentially leads to the evolution of benign interactions. We studied the demographic and behavioral traits of the ant social parasite Megalomyrmex symmetochus (Solenopsidini), an agro-predator that feeds on larvae and fungal garden products of their host, Sericomyrmex amabilis (Attini). Based on demographic data from 15 parasitized colonies, the proportion of parasitic workers to those of the host is 1:2. Moreover, defensive prophylactic behaviors observed during infections with Metarhizium brunneum, a generalist entomopathogen, and Escovopsis, a specialized fungal garden parasite, showed that S. amabilis works extensively to remove and control fungal infections, in contrast to M. symmetochus. M. symmetochus, however, performed intraspecific allogrooming during infections with Escovopsis and M. brunneum, suggesting that they may recognize fungal pathogens and indirectly limit dispersion of spores. Our results indicate that M. symmetochus did not have a strong role in maintaining a hygienic nest.
[Show abstract][Hide abstract] ABSTRACT: Leaf-cutter ants Atta colombica form supply chains to move leaf fragments from their foraging sites to the nest of the colony. The ants then mulch these leaf fragments into substrate for the fungus they grow for food. The overall efficiency of this transportation system depends on the dynamic integration of the supply rate of the cutter ants, the layout of the trail network and the processing rate of the workers remaining at the nest. In this study, we investigated the contribution of leaf-caches (way stations that can form near the production sites, along the trail, and near the nest) to the foraging efficiency of natural colonies. In this study we tested to see if these leaf-caches were used as buffers to equalize flow rate when leaf delivery and processing rate were mismatched. The nutritional quality of the leaves is important for fungal growth. Therefore, we also tested the cycling of leaves within caches to investigate whether fresh leaves are prioritized and how this occurs. Results from this study have important implications for our understanding of the caching behavior of leaf-cutting ants and the optimization of self-organizing supply chains.
Entomological Society of America Annual Meeting 2013; 11/2013
[Show abstract][Hide abstract] ABSTRACT: Over the past decade, there has been growing evidence that non-human animals maintain individual personalities, or sets of behavioral tendencies that are consistent across contexts, a phenomenon termed behavioral syndromes. This framework shifts the classic approach to behavioral ecology by implying limited behavioral flexibility. To account for this, behavioral traits should be viewed across multiple situations instead of in isolated contexts, aiming to quantify individual variation instead of ignoring it. Studies in a broad range of taxa (e.g., birds, fish, and spiders) have described behavioral syndromes in individuals, but collective behavioral syndromes of highly social groups are largely uncharted. These groups provide an opportune system for studying the proximate and ultimate mechanisms driving behavioral syndromes because colonies can be easily manipulated and deconstructed. We tested for the existence of collective behavioral syndromes in ant colonies of an arboreal Azteca ant associated with Cecropia trees. Preliminary evidence shows consistent variation in defensive behavior among colonies, suggesting collective behavioral syndromes may occur. Pursuing this, we presented colonies with a series of behavioral tests to assess five colony-level behavioral traits: defensive aggression, exploratory tendency, prey capture efficiency, response to leaf damage, and patrolling behavior. This work sets up future studies that will focus on how the personalities of a colony’s workers influence its collective personality, environmental effects on colony personality, and fitness consequences of behavioral type.
Entomological Society of America Annual Meeting 2013; 11/2013
[Show abstract][Hide abstract] ABSTRACT: Associative color learning has been demonstrated to be very poor using restrained European honey bees unless the antennae are amputated. Consequently, our understanding of proximate mechanisms in visual information processing is handicapped. Here we test learning performance of Africanized honey bees under restrained conditions with visual and olfactory stimulation using the proboscis extension response (PER) protocol. Restrained individuals were trained to learn an association between a color stimulus and a sugar-water reward. We evaluated performance for "absolute" learning (learned association between a stimulus and a reward) and "discriminant" learning (discrimination between two stimuli). Restrained Africanized honey bees (AHBs) readily learned the association of color stimulus for both blue and green LED stimuli in absolute and discriminatory learning tasks within 7 presentations, but not with violet as the rewarded color. Additionally, 24-hour memory improved considerably during the discrimination task, compared to absolute association (15%-55%). We found that antennal amputation was unnecessary and reduced performance in AHBs. Thus color learning can now be studied using the PER protocol with intact AHBs. This finding opens the way toward investigating visual and multimodal learning with application of neural techniques commonly used in restrained honey bees.
[Show abstract][Hide abstract] ABSTRACT: Fungal symbionts that live asymptomatically inside plant tissues (endophytes) can influence plant–insect interactions. Recent work has shown that damage by leaf-cutting ants, a major Neotropical defoliator, is reduced to almost half in plants with high densities of endophytes. We investigated changes in the phenotype of leaves that could influence ants' behavior to result in the reduction of foliar damage.
We produced cucumber seedlings with high and low densities of one common endophyte species, Colletotrichum tropicale. We used the leaves in bioassays and to compare chemical and physical leaf characteristics important for ants' food selection.
Ants cut about one-third more area of cucumber leaves with lower densities of endophytes and removed c. 20% more paper disks impregnated with the extracts of those leaves compared with leaves and disks from plants hosting the fungus. Colletotrichum tropicale colonization did not cause detectable changes in the composition of volatile compounds, cuticular waxes, nutrients or leaf toughness.
Our study shows that endophytes changed leaf chemistry and suggests that compounds with relative low volatility released after leaf wounding are a major factor influencing foraging decisions by ants when choosing between plants with low or high endophyte loads.
New Phytologist 04/2013; 198(1):241-51. DOI:10.1111/nph.12140 · 7.67 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The genus Mycocepurus is a phylogenetically basal attine ant, so studies of its biology may provide insight into the evolution of behaviours associated with fungus‐growing that characterize the tribe Attini. Mycocepurus smithii from Puerto Rico produces sexual females from July to September, but no males were observed in 2 years of observations, confirming previous observations elsewhere. Colonies were founded between July and August and most nests were haplometrotic (85% of 74 nests). After excavating a tunnel and small chamber, a foundress queen inserted her fore wings into the ceiling and used the wing surfaces as a platform on which the incipient fungal garden was grown. Foundresses foraged for substrate to grow the fungus garden. Growth of incipient colonies was slow: the first workers emerged 2–5 months after colony founding and, after 8 months, colonies contained on average only a single worker.
Journal of Natural History 02/2013; 39:1735-1743. DOI:10.1080/00222930400027462 · 0.93 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Local environmental conditions can facilitate or preclude the development of eusocial colonies in insects that facultatively express behavioural-caste polyphenism. To explore how environmental variability relates to the expression of social behaviour, we collected 120 nests of the facultatively social sweat bee, Megalopta
genalis (Halictidae: Augochlorini), along a nearly twofold rainfall gradient in central Panama. Brood rearing activity of bees in seasonal neotropical forests should track flowering phenologies, which are typically set by rainfall and phylogenetic patterns. Nests were collected at roughly similar times of year from three sites comprising wet, moist and dry lowland tropical forests. There were significant differences in ovarian development, brood production and body size across sites for some comparisons, but no effect on the proportion of social colonies collected at each site. Results show that phenotypes of M. genalis relevant to social behaviour (ovarian development, brood production, body size) may be responsive to variation in local environment over distances of <20 km.
[Show abstract][Hide abstract] ABSTRACT: The reproductive (queen) and nonreproductive (worker) castes of eusocial insect colonies are a classic example of insect polyphenism. A complementary polyphenism may also exist entirely among females in the reproductive caste. Although less studied, reproductive females may vary in behavior based on size-associated attributes leading to the production of daughter workers. We studied a bee with flexible social behavior, Megalopta genalis, to better understand the potential of this polyphenism to shape the social organization of bee colonies and, by extension, its role in the evolution of eusociality. Our experimental design reduced variation among nest foundresses in life history variables that could influence reproductive decisions, such as nesting quality and early adulthood experience. Within our study population, approximately one third of M. genalis nests were eusocial and the remaining nests never produced workers. Though they do not differ in survival, nest-founding females who do not attempt to produce workers (which we refer to as the solitary phenotype) are significantly smaller and become reproductive later than females who attempt to recruit workers (the social phenotype). Females with the social phenotype are more likely to produce additional broods but at a cost of having some of their first offspring become nonreproductive workers. The likelihood of eusocial organization varies with body size across females of the social phenotype. Thus, fitness consequences associated with size-based plasticity in foundress behavior has colony level effects on eusociality. The potential for size-based polyphenisms among reproductive females may be an important factor to consider in the evolutionary origins of eusociality.
[Show abstract][Hide abstract] ABSTRACT: Background
Previous work has shown that leaf-cutting ants prefer to cut leaf material with relatively low fungal endophyte content. This preference suggests that fungal endophytes exact a cost on the ants or on the development of their colonies. We hypothesized that endophytes may play a role in their host plants’ defense against leaf-cutting ants. To measure the long-term cost to the ant colony of fungal endophytes in their forage material, we conducted a 20-week laboratory experiment to measure fungal garden development for colonies that foraged on leaves with low or high endophyte content.
Colony mass and the fungal garden dry mass did not differ significantly between the low and high endophyte feeding treatments. There was, however, a marginally significant trend toward greater mass of fungal garden per ant worker in the low relative to the high endophyte treatment. This trend was driven by differences in the fungal garden mass per worker from the earliest samples, when leaf-cutting ants had been foraging on low or high endophyte leaf material for only 2 weeks. At two weeks of foraging, the mean fungal garden mass per worker was 77% greater for colonies foraging on leaves with low relative to high endophyte loads.
Our data suggest that the cost of endophyte presence in ant forage material may be greatest to fungal colony development in its earliest stages, when there are few workers available to forage and to clean leaf material. This coincides with a period of high mortality for incipient colonies in the field. We discuss how the endophyte-leaf-cutter ant interaction may parallel constitutive defenses in plants, whereby endophytes reduce the rate of colony development when its risk of mortality is greatest.
[Show abstract][Hide abstract] ABSTRACT: The evolution of eusociality is hypothesized to have involved de-coupling parental care from reproduction mediated by changes in endocrine regulation. While data for obligately eusocial insects are consistent with this hypothesis, we lack information from species representative of the transition from solitary reproduction to eusociality. Here we report the first evidence for a link between endocrine processes and social behavior in a facultatively eusocial bee, Megalopta genalis (Halictidae). Using females that varied in social, reproductive, and ecological context, we measured juvenile hormone (JH), a major regulator of colony caste dynamics in other eusocial species. JH was low at adult emergence, but elevated after 10days in all nesting females. Females reared in cages with ad lib nutrition, however, did not elevate JH levels after 10days. All reproductive females had significantly more JH than all age-matched non-reproductive females, suggesting a gonadotropic function. Among females in established nests, JH was higher in queens than workers and solitary reproductives, suggesting a role for JH in social dominance. A lack of significant differences in JH between solitary reproductives and non-reproductive workers suggests that JH content reflects more than reproductive status. Our data support the hypothesis that endocrine modifications are involved in the evolutionary decoupling of reproductive and somatic effort in social insects. These are the first measurements of JH in a solitary-nesting hymenopteran, and the first to compare eusocial and solitary nesting individuals of the same species.
Hormones and Behavior 09/2012; 63(1). DOI:10.1016/j.yhbeh.2012.08.012 · 4.51 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Background/Question/Methods
Plants and insects host a wide diversity of symbiotic fungi, with some symbionts being essential to host survival. Previous studies have focused largely on the reciprocal costs and benefits within a particular host-symbiont pair, but have rarely investigated the multiple interactions among pairs of symbionts and their hosts. Because most organisms participate in symbioses, such symbiont-symbiont interactions must occur often but in a cryptic fashion. Our research focuses on the fungal-fungal interactions among two symbiotic pairs: (i) leaf-cutting ants and their symbiotic fungal gardens, and (ii) tropical plants and their foliar endophytes, the cryptic symbiotic fungi within their leaf tissue. Previous work has shown that leaf-cutting ants prefer to cut leaf material that is relatively low in fungal endophyte content. Such a preference suggests that fungal endophytes exact a cost on the ants or on the development of their colonies. It also suggests that endophytes may play a factor in their host plants’ defense against leaf-cutting ants. To measure the cost to the ant colony of fungal endophytes in their forage material, we conducted a 20-week laboratory experiment to measure fungal garden development for colonies that foraged on leaves with low and high endophyte content.
We found that the colony mass and the fungal garden dry mass did not differ significantly between the low and high endophyte feeding treatments. There was, however, a marginally significant trend toward greater mass of fungal garden per ant worker in the low relative to the high endophyte treatment. This trend was driven by differences in the fungal garden mass per worker in the earliest samples, when leaf-cutting ants had been foraging on low and high endophyte leaf material for only 2 weeks. At two weeks of foraging, the mean fungal garden mass per worker was 77% greater for colonies foraging on leaves with low relative to high endophyte loads. Our data suggest that the cost of endophyte presence in ant forage material may be greatest to fungal colony development in its earliest stages, when there are few workers available to forage and to clean leaf material. This coincides with a period of high mortality for incipient colonies in the field. We discuss how the endophyte-leaf-cutter ant interaction may parallel constitutive defenses in plants, whereby endophytes reduce the rate of colony development when its risk of morality is greatest.
[Show abstract][Hide abstract] ABSTRACT: 1. Fungal endophytes are microfungi that reside asymptomatically inside of leaf tissues, increasing in density and diversity through time after leaves flush. Previous studies have suggested that the presence of fungal endophytes in the harvest material of leaf‐cutting ants (Atta colombica, Guérin‐Méneville) may negatively affect the ants and their fungal cultivar.2. In the present study, it was tested whether the presence and diversity of fungal endophytes affected the amount of time necessary for leaf‐cutter ants to cut, process, and plant leaf material in their fungal garden. It was found that ants took 30–43% longer to cut, carry, clean, and plant leaf tissue with high relative to low endophyte abundance, and that the ants responded similarly to leaf tissue with high or low endophyte diversity.3. It was further investigated whether the fungal cultivars' colonisation rate was greater on leaf material without fungal endophytes. No difference in the ants' cultivar colonisation rate on leaf tissue with high or low endophyte abundance was observed.