Evolution of Cooperation

Salzman S, Crook D, Crall JD, Hopkins R, Pierce NE. An ancient push-pull pollination mechanism in cycads. Science Advances. 2020;6 (24). salzman_cycads_2020.pdf
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.
Cheng D, Chen S, Huang Y, Pierce NE, Riegler M, Yang F, Zeng L, Lu Y, Liang G, Xu Y. Symbiotic microbiota may reflect host adaptation by resident to invasive ant species. PLOS Pathogens. 2019;15 (7). cheng_microbiota_2019.pdf
Boyle JH, Martens D, Musili PM, Pierce NE. Population Genomics and Demographic Sampling of the Ant-Plant Vachellia drepanolobium and Its Symbiotic Ants From Sites Across Its Range in East Africa. Frontiers in Ecology and Evolution. 2019;7. boyle_drepanolobium2019.pdf
Rubin BE, Sanders JG, Turner KM, Pierce NE, Kocher SD. Social behavior in bees influences the abundance of Sodalis (Enterobacteriaceae) symbionts. Royal Society Open Science. 2018. rubin_sodalis.pdf
Bisch G, Minna-Maria Neuvonen MM, Pierce NE, J.A. R, Koga R, Sanders JG, Łukasik P, Andersson SGE. Genome evolution of Bartonellaceae symbionts of ants at the opposite ends of the trophic scale. Genome Biology and Evolution. 2018. bisch_barton.pdf
Kocher SD, Mallarino R, Rubin ER, Yu DW, Hoekstra HE, Pierce NE. The genetic basis of a social polymorphism in halictid bees. Nature Communications. 2018. kocher_poly.pdf
Wittwer B, Hefetz A, Simon T, Murphy LEK, Elgar MA, Pierce NE, Kocher SD. Solitary bees reduce investment in communication compared with their social relatives. Proceedings of the National Academy of Science USA. 2017;114 :6569–6574. Publisher's Version pnas-2017-wittwer-6569-74.pdf
Baker CCM, Martins DJ, Pelaez JN, Billen JPJ, Pringle A, Frederickson ME, Pierce NE. Distinctive fungal communities in an obligate African ant plant mutualism. Proceedings of the Royal Society B. 2017;284 (20162501). Publisher's Version 20162501.full_.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 

Hojo MK, Pierce NE, Tsuji K. Lycaenid Caterpillar Secretions Manipulate Attendant Ant Behavior. Current Biology. 2015;25 :2260-2264.Abstract

Mutualistic interactions typically involve the exchange of different commodities between species [1]. Nutritious secretions are produced by a number of insects and plants in exchange for services such as defense [2, 3]. These rewards are valuable metabolically and can be used to reinforce the behavior of symbiotic partners that can learn and remember them effectively [4, 5]. We show here novel effects of insect exocrine secretions produced by caterpillars in modulating the behavior of attendant ants in the food-for-defense interaction between lycaenid butterflies and ants [6]. Reward secretions from the dorsal nectary organ (DNO) of Narathura japonica caterpillars function to reduce the locomotory activities of their attendant ants, Pristomyrmex punctatus workers. Moreover, workers that feed from caterpillar secretions are significantly more likely to show aggressive responses to eversion of the tentacle organs of the caterpillars. Analysis of the neurogenic amines in the brains of workers that consumed caterpillar secretions showed a significant decrease in levels of dopamine compared with controls. Experimental treatments in which reserpine, a known inhibitor of dopamine in Drosophila, was fed to workers similarly reduced their locomotory activity. We conclude that DNO secretions of lycaenid caterpillars can manipulate attendant ant behavior by altering dopaminergic regulation and increasing partner fidelity. Unless manipulated ants also receive a net nutritional benefit from DNO secretions, this suggests that similar reward-for-defense interactions that have been traditionally considered to be mutualisms may in fact be parasitic in nature.

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.

Archetti M, Scheuring I, Hoffman M, Frederickson ME, Pierce NE, Yu DW. Economic game theory for mutualism and cooperation. Ecology Letters. 2011;14 :1300-1312.Abstract

We review recent work at the interface of economic game theory and evolutionary biology that provides new insights into the evolution of partner choice, host sanctions, partner fidelity feedback and public goods. (1) The theory of games with asymmetrical information shows that the right incentives allow hosts to screen-out parasites and screen-in mutualists, explaining successful partner choice in the absence of signalling. Applications range from ant-plants to microbiomes. (2) Contract theory distinguishes two longstanding but weakly differentiated explanations of host response to defectors: host sanctions and partner fidelity feedback. Host traits that selectively punish misbehaving symbionts are parsimoniously interpreted as pre-adaptations. Yucca-moth and legume-rhizobia mutualisms are argued to be examples of partner fidelity feedback. (3) The theory of public goods shows that cooperation in multi-player interactions can evolve in the absence of assortment, in one-shot social dilemmas among non-kin. Applications include alarm calls in vertebrates and exoenzymes in microbes.

Archetti M, Ubeda F, Fudenberg D, Green J, Pierce NE, Yu DW. Let the Right One In: A Microeconomic Approach to Partner Choice in Mutualisms. American Naturalist. 2011;177 :75-85.Abstract

One of the main problems impeding the evolution of cooperation is partner choice. When information is asymmetric (the quality of a potential partner is known only to himself), it may seem that partner choice is not possible without signaling. Many mutualisms, however, exist without signaling, and the mechanisms by which hosts might select the right partners are unclear. Here we propose a general mechanism of partner choice, "screening," that is similar to the economic theory of mechanism design. Imposing the appropriate costs and rewards may induce the informed individuals to screen themselves according to their types and therefore allow a noninformed individual to establish associations with the correct partners in the absence of signaling. Several types of biological symbioses are good candidates for screening, including bobtail squid, ant-plants, gut microbiomes, and many animal and plant species that produce reactive oxygen species. We describe a series of diagnostic tests for screening. Screening games can apply to the cases where by-products, partner fidelity feedback, or host sanctions do not apply, therefore explaining the evolution of mutualism in systems where it is impossible for potential symbionts to signal their cooperativeness beforehand and where the host does not punish symbiont misbehavior.

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.

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.

Eastwood R, Pierce NE, Kitching RL, Hughes JM. Do ants enhance diversification in lycaenid butterflies? Phylogeographic evidence from a model myrmecophile, Jalmenus evagoras. Evolution. 2006;60 :315-327.Abstract

Abstract. The ant-tended Australian butterfly, Jalmenus evagoras, has been a model system for studying the ecology and evolution of mutualism. A phylogeographic analysis of mitochondrial DNA cytochrome oxidase I sequences from 242 butterflies (615 bp) and 66 attendant ants (585 bp) from 22 populations was carried out to explore the relationship between ant association and butterfly population structure. This analysis revealed 12 closely related butterfly haplotypes in three distinct clades roughly corresponding to three allopatric subpopulations of the butterflies. Minimal genetic diversity and widespread haplotypes within biogeographical regions suggest high levels of matrilineal gene flow. Attendant ants are significantly more diverse than was previously thought, with at least seven well-defined clades corresponding to independent morphological determinations, distributed throughout the range of the butterflies. Nested analysis of molecular variance showed that biogeography, host plant, and ant associate all contribute significantly in explaining variation in butterfly genetic diversity, but these variables are not independent of one another. Major influences appear to come from fragmentation due to large-scale biogeographical barriers, and diversification following a shift in habitat preference. A consequence of such a shift could be codiversification of the butterfly with habitatadapted ants, resulting in apparent phylogenetic concordance between butterflies and ants. The implications of these results are discussed in terms of possible effects of ant attendance on the diversification of Lycaenidae as a whole.

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.

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.