Behavioral Ecology

2016
Elgar MA, Nash DR, Pierce NE. Eavesdropping on cooperative communication within an ant-butterfly mutualism. The Science of Nature [Internet]. 2016;103 :84. Publisher's VersionAbstract

DOI 10.1007/s00114-016-1409-5 

eavesdropping.pdf
2014
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.

2014_price_et_al.pdf
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.

2014_kocher_et_al.pdf
2013
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.

2013_kronauer_et_al.pdf
2011
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.

2011_funaro_et_al.pdf
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.

2011_ramirez_et_al.pdf
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
2010
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.

pnas-2010-weyl-15712-6.pdf
2009
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.

2009_russell_et_al.pdf
2008
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.

2008_travassos_et_al.pdf
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.

2008_mathew_et_al.pdf
2006
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.

2006_lohman_et_al.pdf
2004
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.

2004_quek_et_al.pdf
Als TD, Vila R, Kandul NP, Nash DR, Yen SH, Hsu YF, Mignault AA, Boomsma JJ, Pierce NE. The evolution of alternative parasitic life histories in large blue butterflies. Nature. 2004;432 :386-390.Abstract

Large blue (Maculinea) butterflies are highly endangered throughout the Palaearctic region, and have been the focus of intense conservation research(1-3). In addition, their extraordinary parasitic lifestyles make them ideal for studies of life history evolution. Early instars consume flower buds of specific host plants, but later instars live in ant nests where they either devour the brood (predators), or are fed mouth-to-mouth by the adult ants (cuckoos). Here we present the phylogeny for the group, which shows that it is a monophyletic clade nested within Phengaris, a rare Oriental genus whose species have similar life histories(4,5). Cuckoo species are likely to have evolved from predatory ancestors. As early as five million years ago, two Maculinea clades diverged, leading to the different parasitic strategies seen in the genus today. Contrary to current belief, the two recognized cuckoo species show little genetic divergence and are probably a single ecologically differentiated species(6-10). On the other hand, some of the predatory morphospecies exhibit considerable genetic divergence and may contain cryptic species. These findings have important implications for conservation and reintroduction efforts.

2004_als_et_al.pdf
2002
Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annual Review of Entomology. 2002;47 :733-771.Abstract

The estimated 6000 species of Lycaenidae account for about one third of all Papilionoidea. The majority of lycaenids have associations with ants that can be facultative or obligate and range from mutualism to parasitism. Lycaenid larvae and pupae employ complex chemical and acoustical signals to manipulate ants. Cost/benefit analyses have demonstrated multiple trade-offs involved in myrmecophily. Both demographic and phylogenetic evidence indicate that ant association has shaped the evolution of obligately associated groups. Parasitism typically arises from mutualism with ants, arid entomophagous species are disproportionately common in the Lycaenidae compared with other Lepidoptera. Obligate associations are more common in the Southern Hemisphere, in part because highly ant-associated lineages make up a larger proportion of the fauna in these, regions. Further research on phylogeny and natural history, particularly of the Neotropical fauna, will be necessary to understand the rote ant association has played in the evolution of the Lycaenidae.

2002_pierce_et_al.pdf
Fraser AM, Tregenza T, Wedell N, Elgar MA, Pierce NE. Oviposition tests of ant preference in a myrmecophilous butterfly. Journal of Evolutionary Biology. 2002;15 :861-870.Abstract

Butterflies in the family Lycaenidae that have obligate associations with ants frequently exhibit ant-dependent egg laying behaviour. In a series of field and laboratory choice tests, we assessed oviposition preference of the Australian lycaenid Jalmenus evagoras in response to different species and populations of ants. Females discriminated between attendant and nonattendant ant species, between attendant ant species, and to some extent, between populations of a single ant species. When preferences were found, ovipositing butterflies preferred their locally predominant attendant ant species and geographically proximate attendant ant populations. A reciprocal choice test using adults from a generation of butterflies reared in the absence of ants indicated a genetic component to oviposition preference. Individual females were flexible with respect to oviposition site choice, often ovipositing on more than one treatment during a trial. Preferences arose from a hierarchical ranking of ant treatments. These results are discussed in terms of local adaptation and its possible significance in the diversification of ant-associated lycaenids.

2002_fraser_et_al.pdf
2001
Pierce NE. Peeling the onion: Symbioses between ants and blue butterflies. In: Model systems in behavioral ecology. Princeton: Princeton University Press ; 2001. pp. 41-56. 2001_pierce_peeling_the_onion.pdf
Fraser AM, Axen AH, Pierce NE. Assessing the quality of different ant species as partners of a myrmecophilous butterfly. Oecologia. 2001;129 :452-460.Abstract

We assessed the quality of different ant species as partners of the facultatively myrmecophilous lycaenid butterfly Glaucopsyche lygdamus. We compared disappearance and parasitism rates of G. lygdamus larvae in the field, and development of non-feeding pre-pupae in the laboratory, when individuals were untended or tended by one of four ant species. Formica podzolica was the only ant species to provide a clear benefit to G. lygdamus, in the form of reduced larval parasitism relative to untended larvae. F. 'neogagates' (F. neogagates + F. lasioides) and Tapinoma sessile were essentially neutral partners, providing no significant cost or benefit for any of the parameters measured. Relative to untended individuals, association with F. obscuripes significantly increased larval disappearance and significantly decreased pupal mass. Thus, F. obscuripes may act as a parasite of the general association between G. lygdamus and ants under certain conditions. Ant species also differed in their persistence as tenders of G. lygdamus larvae once an interaction was established. Over the lifetime of a larva, F. podzolica and F. obscuripes usually remained as the attendant ant species on plants over consecutive census dates, while F. 'neogagates' and T. sessile were frequently replaced, most commonly by F. obscuripes. It remains to be determined if disappearance and developmental outcomes reported here reflect true fitness costs (i.e. reduced survivorship and lower reproductive success) for G. lygdamus. The potential and limitations for specialization in association between G. lygdamus and high quality ant partners are discussed.

2001_fraser_et_al.pdf
Pratt SC, Pierce NE. The cavity-dwelling ant Leptothorax curvispinosus uses nest geometry to discriminate between potential homes. Animal Behaviour. 2001;62 :281-287.Abstract

Nest site selection is a frequent context for decision making in ants, but little is known of the criteria used to make a choice. We tested the nest site preferences of Leptothorax curvispinosus, both by measuring hollow acorn nests occupied in nature, and by inducing laboratory colonies to choose between artificial nests of different design. Three criteria were examined. (1) Entrance size: the ants preferred small entrance holes, presumably for their greater defensibility and crypsis. Natural nest entrances were small, and 52% of them were reduced still further by the addition of rims of soil and leaf litter. In choice tests, colonies selected nest entrances near the median size of rimmed natural holes, rejecting those near the larger end of the distribution of raw natural holes. (2) Cavity volume: acorn cavity volume was weakly correlated with the size of the occupying colony. In choice tests, colonies rejected cavities near the median size of natural nests, preferring instead larger cavities near the upper end of the natural size distribution. This may reflect active size matching of colonies to nests, because the colonies used in the choice test were bigger than those from the natural nest sample. Alternatively, all colonies may prefer big nests, but face limited availability of large cavities in nature. (3) Cavity shape: colonies preferred shapes roughly similar to that of an acorn interior, rejecting thin crevices in favour of compact, high-ceilinged cavities. (C) 2001 The Association for the Study of Animal Behaviour.

2001_pratt_pierce.pdf

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