Behavioral Ecology

Malé PJG, Youngerman E, Pierce NE, Frederickson ME. Mating system, population genetics, and phylogeography of the devil’s garden ant, Myrmelachista schumanni, in the Peruvian Amazon. Insectes Sociaux. 2020;67 :113-125.
Tsai C-C, Childers RA, Shi NN, Ren C, Pelaez JN, Bernard GD, Pierce NE, Yu N. Physical and behavioral adaptations to prevent overheating of the living wings of butterflies. Nature Communications. 2020;11. tsai_overheating_2020.pdf
Crall JD, Switzer CM, Oppenheimer RL, Ford Versypt AN, Dey B, Brown A, Eyster M, Guerin C, Pierce NE, Combes SA, et al. Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science. 2018;362 (6415) :683-686. crall_neonicotinoid.pdf
Crall JD, Kocher S, Oppenheimer RL, Gravish N, Mountcastle AM, Pierce NE, Combes SA. Spatial fidelity of workers predicts collective response to disturbance in a social insect. Nature Communications. 2018;9 (1201). crall_et_al_2018_s41467-018-03561-w.pdf
Boyle JH, Martins DJ, Peleaz J, Musili PM, Kibet S, Ndung’u KN, Kenfack D, Pierce NE. Polygyny cannot explain the superior competitive ability of dominant ant associates in the African ant plant Acacia(Vachellia) drepanolobium. Ecology and Evolution. 2017;8 :1441-1450. boyle_et_al_2017_ece3-8-1441.pdf
Elgar MA, Nash DR, Pierce NE. Eavesdropping on cooperative communication within an ant-butterfly mutualism. The Science of Nature . 2016;103 :84. Publisher's VersionAbstract

DOI 10.1007/s00114-016-1409-5 

Price SL, Powell S, Kronauer DJC, Tran LAP, Pierce NE, Wayne RK. Renewed diversification is associated with new ecological opportunity in the Neotropical turtle ants. Journal of Evolutionary Biology. 2014;27 :242-258.Abstract

Ecological opportunity, defined as access to new resources free from competitors, is thought to be a catalyst for the process of adaptive radiation. Much of what we know about ecological opportunity, and the larger process of adaptive radiation, is derived from vertebrate diversification on islands. Here, we examine lineage diversification in the turtle ants (Cephalotes), a species-rich group of ants that has diversified throughout the Neotropics. We show that crown group turtle ants originated during the Eocene (around 46 mya), coincident with global warming and the origin of many other clades. We also show a marked lineage-wide slowdown in diversification rates in the Miocene. Contrasting this overall pattern, a species group associated with the young and seasonally harsh Chacoan biogeographic region underwent a recent burst of diversification. Subsequent analyses also indicated that there is significant phylogenetic clustering within the Chacoan region and that speciation rates are highest there. Together, these findings suggest that recent ecological opportunity, from successful colonization of novel habitat, may have facilitated renewed turtle ant diversification. Our findings highlight a central role of ecological opportunity within a successful continental radiation.

Kocher SD, Pellissier L, Veller C, Purcell J, Nowak MA, Chapuisat M, Pierce NE. Transitions in social complexity along elevational gradients reveal a combined impact of season length and development time on social evolution. Proceedings of the Royal Society B-Biological Sciences. 2014;281.Abstract

Eusociality is taxonomically rare, yet associated with great ecological success. Surprisingly, studies of environmental conditions favouring eusociality are often contradictory. Harsh conditions associated with increasing altitude and latitude seem to favour increased sociality in bumblebees and ants, but the reverse pattern is found in halictid bees and polistine wasps. Here, we compare the life histories and distributions of populations of 176 species of Hymenoptera from the Swiss Alps. We show that differences in altitudinal distributions and development times among social forms can explain these contrasting patterns: highly social taxa develop more quickly than intermediate social taxa, and are thus able to complete the reproductive cycle in shorter seasons at higher elevations. This dual impact of altitude and development time on sociality illustrates that ecological constraints can elicit dynamic shifts in behaviour, and helps explain the complex distribution of sociality across ecological gradients.

Kronauer DJC, Tsuji K, Pierce NE, Keller L. Non-nest mate discrimination and clonal colony structure in the parthenogenetic ant Cerapachys biroi. Behavioral Ecology. 2013;24 :617-622.Abstract

Understanding the interplay between cooperation and conflict in social groups is a major goal of biology. One important factor is genetic relatedness, and animal societies are usually composed of related but genetically different individuals, setting the stage for conflicts over reproductive allocation. Recently, however, it has been found that several ant species reproduce predominantly asexually. Although this can potentially give rise to clonal societies, in the few well-studied cases, colonies are often chimeric assemblies of different genotypes, due to worker drifting or colony fusion. In the ant Cerapachys biroi, queens are absent and all individuals reproduce via thelytokous parthenogenesis, making this species an ideal study system of asexual reproduction and its consequences for social dynamics. Here, we show that colonies in our study population on Okinawa, Japan, recognize and effectively discriminate against foreign workers, especially those from unrelated asexual lineages. In accord with this finding, colonies never contained more than a single asexual lineage and average pairwise genetic relatedness within colonies was extremely high (r = 0.99). This implies that the scope for social conflict in C. biroi is limited, with unusually high potential for cooperation and altruism.

Funaro CF, Kronauer DJC, Moreau CS, Goldman-Huertas B, Pierce NE, Russell JA. Army Ants Harbor a Host-Specific Clade of Entomoplasmatales Bacteria. Applied and Environmental Microbiology. 2011;77 :346-350.Abstract

In this article, we describe the distributions of Entomoplasmatales bacteria across the ants, identifying a novel lineage of gut bacteria that is unique to the army ants. While our findings indicate that the Entomoplasmatales are not essential for growth or development, molecular analyses suggest that this relationship is host specific and potentially ancient. The documented trends add to a growing body of literature that hints at a diversity of undiscovered associations between ants and bacterial symbionts.

Ramirez SR, Eltz T, Fujiwara MK, Gerlach G, Goldman-Huertas B, Tsutsui ND, Pierce NE. Asynchronous Diversification in a Specialized Plant-Pollinator Mutualism. Science. 2011;333 :1742-1746.Abstract

Most flowering plants establish mutualistic associations with insect pollinators to facilitate sexual reproduction. However, the evolutionary processes that gave rise to these associations remain poorly understood. We reconstructed the times of divergence, diversification patterns, and interaction networks of a diverse group of specialized orchids and their bee pollinators. In contrast to a scenario of coevolution by race formation, we show that fragrance-producing orchids originated at least three times independently after their fragrance-collecting bee mutualists. Whereas orchid diversification has apparently tracked the diversification of orchids' bee pollinators, bees appear to have depended on the diverse chemical environment of neotropical forests. We corroborated this apparent asymmetrical dependency by simulating co-extinction cascades in real interaction networks that lacked reciprocal specialization. These results suggest that the diversification of insect-pollinated angiosperms may have been facilitated by the exploitation of preexisting sensory biases of insect pollinators.

Kronauer DJC, Pierce NE. Myrmecophiles. Current Biology. 2011;21 :R208-R209. 2011_kronauer_and_pierce.pdf
Weyl EG, Frederickson ME, Yu DW, Pierce NE. Reply to Kiers et al.: Economic and biological clarity in the theory of mutualism. Proceedings of the National Academy of Sciences of the United States of America. 2011;108 :E8-E8. 2011_weyl_et_al_reply.pdf
Weyl EG, Frederickson ME, Yu DW, Pierce NE. Economic contract theory tests models of mutualism. Proceedings of the National Academy of Sciences. 2010;107 (36) :15712-15716.Abstract

Although mutualisms are common in all ecological communities and have played key roles in the diversification of life, our current understanding of the evolution of cooperation applies mostly to social behavior within a species. A central question is whether mutualisms persist because hosts have evolved costly punishment of cheaters. Here, we use the economic theory of employment contracts to formulate and distinguish between two mechanisms that have been proposed to prevent cheating in host–symbiont mutualisms, partner fidelity feedback (PFF) and host sanctions (HS). Under PFF, positive feedback between host fitness and symbiont fitness is sufficient to prevent cheating; in contrast, HS posits the necessity of costly punishment to maintain mutualism. A coevolutionary model of mutualism finds that HS are unlikely to evolve de novo, and published data on legume–rhizobia and yucca–moth mutualisms are consistent with PFF and not with HS. Thus, in systems considered to be textbook cases of HS, we find poor support for the theory that hosts have evolved to punish cheating symbionts; instead, we show that even horizontally transmitted mutualisms can be stabilized via PFF. PFF theory may place previously underappreciated constraints on the evolution of mutualism and explain why punishment is far from ubiquitous in nature.

Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proceedings of the National Academy of Sciences of the United States of America. 2009;106 :21236-21241.Abstract

Ants are a dominant feature of terrestrial ecosystems, yet we know little about the forces that drive their evolution. Recent findings illustrate that their diets range from herbivorous to predaceous, with "herbivores'' feeding primarily on exudates from plants and sap-feeding insects. Persistence on these nitrogen-poor food sources raises the question of how ants obtain sufficient nutrition. To investigate the potential role of symbiotic microbes, we have surveyed 283 species from 18 of the 21 ant subfamilies using molecular techniques. Our findings uncovered a wealth of bacteria from across the ants. Notable among the surveyed hosts were herbivorous "turtle ants'' from the related genera Cephalotes and Procryptocerus (tribe Cephalotini). These commonly harbored bacteria from ant-specific clades within the Burkholderiales, Pseudomonadales, Rhizobiales, Verrucomicrobiales, and Xanthomonadales, and studies of lab-reared Cephalotes varians characterized these microbes as symbiotic residents of ant guts. Although most of these symbionts were confined to turtle ants, bacteria from an ant-specific clade of Rhizobiales were more broadly distributed. Statistical analyses revealed a strong relationship between herbivory and the prevalence of Rhizobiales gut symbionts within ant genera. Furthermore, a consideration of the ant phylogeny identified at least five independent origins of symbioses between herbivorous ants and related Rhizobiales. Combined with previous findings and the potential for symbiotic nitrogen fixation, our results strongly support the hypothesis that bacteria have facilitated convergent evolution of herbivory across the ants, further implicating symbiosis as a major force in ant evolution.

Travassos MA, Devries PJ, Pierce NE. A novel organ and mechanism for larval sound production in butterfly caterpillars: Eurybia elvina(Lepidoptera: Riodinidae). Tropical Lepidoptera Research. 2008;18 :20-23.Abstract

Abstract – Eurybia elvina larvae produce substrate-borne vibrations by grating a cervical membrane studded with teeth against hemispherical protuberances scattered along the surface of the head.

Mathew J, Travassos MA, Canfield M, Murawski D, Kitching RL, Pierce NE. The singing reaper: diet, morphology and vibrational signaling in the Nearctic species Feniseca tarquinius. Tropical Lepidoptera Research. 2008;18 :24-29.Abstract

Abstract – A survey at fourteen sites in Eastern North America of populations of the carnivorous lycaenid butterfly, Feniseca tarquinius, confirmed that the sole prey item on Alnus rugosa (Betulaceae) for this species in these regions was Paraprociphilus tessellatus (Homoptera: Aphidoidea: Pemphigidae). Overwhelmingly, these aphids were tended by ants in the subfamily Formicinae. These results are compiled with all earlier records of prey aphids, their host plants and attendant ants for this species. SEM examination of a 4th instar larva of F. tarquinius supported Cottrell’s (1984) observation that the dorsal nectary organ and tentacle organs are absent in the 4th instar of virtually all Miletinae. Larvae of F. tarquinius were found to produce substrate-borne vibrations that possess a long pulse length and narrow bandwidth when compared with other lycaenid calls. The possible function of these calls is briefly discussed.

Lohman DJ, Liao Q, Pierce NE. Convergence of chemical mimicry in a guild of aphid predators. Ecological Entomology. 2006;31 :41-51.Abstract

Abstract. 1. A variety of insects prey on honeydew-producing Homoptera and many do so even in the presence of ants that tend, and endeavour to protect, these trophobionts from natural enemies. Few studies have explored the semiochemical mechanisms by which these predators circumvent attack by otherwise aggressive ants. 2. Ants use specific mixtures of cuticular hydrocarbons (CHCs) as recognition labels, but this simple mechanism is frequently circumvented by nest parasites that engage in ‘chemical mimicry’ of their host ants by producing or acquiring a critical suite of these CHCs. 3. Analysis of the CHCs from the North American woolly alder aphid, Prociphilus tessellatus (Homoptera: Aphididae), their tending ants, and aphid predators from three insect orders, Feniseca tarquinius (Lepidoptera: Lycaenidae), Chrysopa slossonae (Neuroptera: Chrysopidae), and Syrphus ribesii (Diptera: Syrphidae), showed that while the CHC profile of each predatory species was distinct, each was chemically more similar to the aphids than to either tending ant species. Further, the CHCs of each predator species were a subset of the compounds found in the aphids’ profile. 4. These results implicate CHCs as a recognition cue used by ants to discriminate trophobionts from potential prey and a probable mechanism by which trophobiont predators circumvent detection by aphids and their tending ants. 5. Although several features of the aphids’ CHC profile are shared among the chemically mimetic taxa, variation in the precision of mimicry among the members of this predatory guild demonstrates that a chemical mimic need not replicate every feature of its model.

Quek SP, Davies SJ, Itino T, Pierce NE. Codiversification in an ant-plant mutualism: Stem texture and the evolution of host use in Crematogaster (Formicidae : Myrmicinae) inhabitants of Macaranga (Euphorbiaceae). Evolution. 2004;58 :554-570.Abstract

We investigate the evolution of host association in a cryptic complex of mutualistic Crematogaster (Decacrema) ants that inhabits and defends Macaranga trees in Southeast Asia. Previous phylogenetic studies based on limited samplings of Decacrema present conflicting reconstructions of the evolutionary history of the association, inferring both cospeciation and the predominance of host shifts. We use cytochrome oxidase I (COI) to reconstruct phylogenetic relationships in a comprehensive sampling of the Decacrema inhabitants of Macaranga. Using a published Macaranga phylogeny, we test whether the ants and plants have cospeciated. The COI phylogeny reveals 10 well-supported lineages and an absence of cospeciation. Host shifts, however, have been constrained by stem traits that are themselves correlated with Macaranga phylogeny. Earlier lineages of Decacrema exclusively inhabit waxy stems, a basal state in the Pachystemon clade within Macaranga, whereas younger species of Pachystemon, characterized by nonwaxy stems, are inhabited only by younger lineages of Decacrema. Despite the absence of cospeciation, the correlated succession of stem texture in both phylogenies suggests that Decacrema and Pachystemon have diversified in association, or codiversified. Subsequent to the colonization of the Pachystemon clade, Decacrema expanded onto a second clade within Macaranga, inducing the development of myrmecophytism in the Pruinosae group. Confinement to the aseasonal wet climate zone of western Malesia suggests myrmecophytic Macaranga are no older than the wet forest community in Southeast Asia, estimated to be about 20 million years old (early Miocene). Our calculation of COI divergence rates from several published arthropod studies that relied on tenable calibrations indicates a generally conserved rate of approximately 1.5% per million years. Applying this rate to a rate-smoothed Bayesian chronogram of the ants, the Decacrema from Macaranga are inferred to be at least 12 million years old (mid-Miocene). However, using the extremes of rate variation in COI produces an age as recent as 6 million years. Our inferred timeline based on 1.5% per million years concurs with independent biogeographical events in the region reconstructed from palynological data, thus suggesting that the evolutionary histories of Decacrema and their Pachystemon hosts have been contemporaneous since the mid-Miocene. The evolution of myrmecophytism enabled Macaranga to radiate into enemy-free space, while the ants' diversification has been shaped by stem traits, host specialization, and geographic factors. We discuss the possibility that the ancient and exclusive association between Decacrema and Macaranga was facilitated by an impoverished diversity of myrmecophytes and phytoecious (obligately plant inhabiting) ants in the region.