Megan E. Frederickson

Economic game theory for mutualism and cooperation.

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.

Economic contract theory tests models of mutualism

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.

Rethinking mutualism stability: cheaters and the evolution of sanctions.

How cooperation originates and persists in diverse species, from bacteria to multicellular organisms to human societies, is a major question in evolutionary biology. A large literature asks: what prevents selection for cheating within cooperative lineages? In mutualisms, or cooperative interactions between species, feedback between partners often aligns their fitness interests, such that cooperative symbionts receive more benefits from their hosts than uncooperative symbionts. But how do these feedbacks evolve? Cheaters might invade symbiont populations and select for hosts that preferentially reward or associate with cooperators (often termed sanctions or partner choice); hosts might adapt to variation in symbiont quality that does not amount to cheating (e.g., environmental variation); or conditional host responses might exist before cheaters do, making mutualisms stable from the outset. I review evidence from yucca-yucca moth, fig-fig wasp, and legume-rhizobium mutualisms, which are commonly cited as mutualisms stabilized by sanctions. Based on the empirical evidence, it is doubtful that cheaters select for host sanctions in these systems; cheaters are too uncommon. Recognizing that sanctions likely evolved for functions other than retaliation against cheaters offers many insights about mutualism coevolution, and about why mutualism evolves in only some lineages of potential hosts.

Ant species confer different partner benefits on two neotropical myrmecophytes

The dynamics of mutualistic interactions involving more than a single pair of species depend on the relative costs and benefits of interaction among alternative partners. The neotropical myrmecophytes Cordia nodosa and Duroia hirsuta associate with several species of obligately symbiotic ants. I compared the ant partners of Cordia and Duroia with respect to two benefits known to be important in ant-myrmecophyte interactions: protection against herbivores provided by ants, and protection against encroaching vegetation provided by ants. Azteca spp., Myrmelachista schumanni, and Allomerus octoarticulatus demerarae ants all provide the leaves of Cordia and Duroia some protection against herbivores. However, Azteca and Allomerus provide more protection than does Myrmelachista to the leaves of their host plants. Although Allomerus protects the leaves of its hosts, plants occupied by Allomerus suffer more attacks by herbivores to their stems than do plants occupied by other ants. Relative to Azteca or Allomerus, Myrmelachista ants provide better protection against encroaching vegetation, increasing canopy openness over their host plants. These differences in benefits among the ant partners of Cordia and Duroia are reflected in the effect of each ant species on host plant size, growth rate, and reproduction. The results of this study show how mutualistic ant partners can differ with respect to both the magnitude and type of benefits they provide to the same species of myrmecophytic host.

Cheaters must prosper: reconciling theoretical and empirical perspectives on cheating in mutualism

Cheating is a focal concept in the study of mutualism, with the majority of researchers considering cheating to be both prevalent and highly damaging. However, current definitions of cheating do not reliably capture the evolutionary threat that has been a central motivation for the study of cheating. We describe the development of the cheating concept and distill a relative-fitness-based definition of cheating that encapsulates the evolutionary threat posed by cheating, i.e. that cheaters will spread and erode the benefits of mutualism. We then describe experiments required to conclude that cheating is occurring and to quantify fitness conflict more generally. Next, we discuss how our definition and methods can generate comparability and integration of theory and experiments, which are currently divided by their respective prioritisations of fitness consequences and traits. To evaluate the current empirical evidence for cheating, we review the literature on several of the best-studied mutualisms. We find that although there are numerous observations of low-quality partners, there is currently very little support from fitness data that any of these meet our criteria to be considered cheaters. Finally, we highlight future directions for research on conflict in mutualisms, including novel research avenues opened by a relative-fitness-based definition of cheating.

The intertwined population biology of two Amazonian myrmecophytes and their symbiotic ants

A major question in ecology is: how do mutualisms between species affect population dynamics? For four years, we monitored populations of two Amazonian myrmecophytes, Cordia nodosa and Duroia hirsuta, and their symbiotic ants. In this system, we investigated how positive feedback between mutualistic plants and ant colonies influenced population processes at two scales: (1) how modular organisms such as plants and ant colonies grew, or eta-demography, and (2) how populations grew, or N-demography. We found evidence of positive feedback between ant colony and plant growth rates. Plants with mutualistic ants (Azteca spp. and Myrmelachista schumanni) grew in a geometric or autocatalytic manner, such that the largest plants grew the most. By contrast, the growth of plants with parasitic ants (Allomerus octoarticulatus) saturated. Ant colonies occupied new domatia as fast as plants produced them, suggesting that mutualistic ant colonies also grew geometrically or autocatalytically to match plant growth. Plants became smaller when they lost ants. While unoccupied, plants continued to become smaller until they had lost all or nearly all their domatia. Hence, the loss of mutualistic ants limited plant growth. C. nodosa and D. hirsuta live longer than their ant symbionts and were sometimes recolonized after losing ants, which again promoted plant growth. Plant growth had fitness consequences for ants and plants; mortality and fecundity depended on plant size. Positive feedback between ants and plants allowed a few plants and ant colonies to become very large; these probably produced the majority of offspring in the next generation.

The Direct and Ecological Costs of an Ant-Plant Symbiosis

How strong is selection for cheating in mutualisms? The answer depends on the type and magnitude of the costs of the mutualism. Here we investigated the direct and ecological costs of plant defense by ants in the association between Cordia nodosa, a myrmecophytic plant, and Allomerus octoarticulatus, a phytoecious ant. Cordia nodosa trees produce food and housing to reward ants that protect them against herbivores. For nearly 1 year, we manipulated the presence of A. octoarticulatus ants and most insect herbivores on C. nodosa in a full-factorial experiment. Ants increased plant growth when herbivores were present but decreased plant growth when herbivores were absent, indicating that hosting ants can be costly to plants. However, we did not detect a cost to ant colonies of defending host plants against herbivores. Although this asymmetry in costs suggests that the plants may be under stronger selection than the ants to cheat by withholding investment in their partner, the costs to C. nodosa are probably at least partly ecological, arising because ants tend scale insects on their host plants. We argue that ecological costs should favor resistance or traits other than cheating and thus that neither partner may face much temptation to cheat.

Conflict over Reproduction in an Ant‐Plant Symbiosis: Why Allomerus octoarticulatus Ants Sterilize Cordia nodosa Trees

The evolutionary stability of mutualism is thought to depend on how well the fitness interests of partners are aligned. Because most ant‐myrmecophyte mutualisms are persistent and horizontally transmitted, partners share an interest in growth but not in reproduction. Resources invested in reproduction are unavailable for growth, giving rise to a conflict of interest between partners. I investigated whether this explains why Allomerus octoarticulatus ants sterilize Cordia nodosa trees. Allomerus octoarticulatus nests in the hollow stem domatia of C. nodosa. Workers protect C. nodosa leaves against herbivores but destroy inflorescences. Using C. nodosa trees with Azteca ants, which do not sterilize their hosts, I cut inflorescences off trees to simulate sterilization by A. octoarticulatus. Sterilized C. nodosa grew faster than control trees, providing evidence for a trade‐off between growth and reproduction. Allomerus octoarticulatus manipulates this trade‐off to its advantage; sterilized trees produce more domatia and can house larger, more fecund colonies.

The devil to pay: a cost of mutualism with Myrmelachista schumanni ants in 'devil's gardens' is increased herbivory on Duroia hirsuta trees

‘Devils gardens’ are nearly pure stands of the myrmecophyte, Duroia hirsuta, that occur in Amazonian rainforests. Devils gardens are created by Myrmelachista schumanni ants, which nest in D. hirsuta trees and kill other plants using formic acid as an herbicide. Here, we show that this ant–plant mutualism has an associated cost; by making devils gardens, M. schumanni increases herbivory on D. hirsuta. We measured standing leaf herbivory on D. hirsuta trees and found that they sustain higher herbivory inside than outside devils gardens. We also measured the rate of herbivory on nursery-grown D. hirsuta saplings planted inside and outside devils gardens in ant-exclusion and control treatments. We found that when we excluded ants, herbivory on D. hirsuta was higher inside than outside devils gardens. These results suggest that devils gardens are a concentrated resource for herbivores. Myrmelachista schumanni workers defend D. hirsuta against herbivores, but do not fully counterbalance the high herbivore pressure in devils gardens. We suggest that high herbivory may limit the spread of devils gardens, possibly explaining why devils gardens do not overrun Amazonian rainforests.

The reproductive phenology of an Amazonian ant species reflects the seasonal availability of its nest sites

In saturated tropical ant assemblages, reproductive success depends on queens locating and competing for scarce nest sites. Little is known about how this process shapes the life histories of tropical ants. Here I investigate the relationship between nest site availability and an important life history trait, reproductive phenology, in the common Amazonian ant species Allomerus octoarticulatus. A. octoarticulatus is a plant-ant that nests in the hollow, swollen stem domatia on Cordia nodosa. I provide evidence that nest sites are limiting for A. octoarticulatus. Most queens produced by A. octoarticulatus colonies died before locating suitable host plants, and most queens that located hosts died before founding colonies, probably from intraspecific competition among queens for control of host plants. I further show that the reproductive phenology of A. octoarticulatus closely matches the seasonal availability of its nest sites, domatia-bearing C. nodosa saplings. Both the production and flight of A. octoarticulatus reproductives, and the number of C. nodosa saplings available for colonization by ants, peaked from March to May. There was correlative evidence that A. octoarticulatus colonies use temperature as a cue to synchronize their reproduction to the availability of C. nodosa saplings: both the production of reproductives by ant colonies and the number of C. nodosa saplings available for colonization were correlated with temperature, and not with rainfall. All of these results suggest that nest site limitation constrains the reproductive phenology of A. octoarticulatus.