Evolution of Mutualism

by

Judith Bronstein

• LAST REVIEWED: 24 September 2020
• LAST MODIFIED: 24 September 2020
• DOI: 10.1093/obo/9780199941728-0128

Introduction

Mutualisms, interactions between two species that benefit both, have long captured the public imagination. Humans are undeniably attracted to the idea of cooperation in nature. For thousands of years we have been seeking explanations for its occurrence in other organisms, often imposing our own motivations and mores in an effort to explain what we see. However, the importance of mutualisms lies much deeper than simply providing material for philosophical treatises and natural history documentaries. The influence of mutualisms transcends levels of biological organization from cells to populations, communities, and ecosystems. Mutualisms were key to the origin of eukaryotic cells and perhaps to the invasion of the land. Mutualisms occur in every aquatic and terrestrial habitat; indeed, ecologists now believe that almost every species on Earth is involved directly or indirectly in one or more of these interactions. Mutualisms are crucial to the reproduction and survival of many plants and animals and to nutrient cycles in ecosystems. Moreover, the ecosystem services mutualists provide (e.g., seed dispersal, pollination, and carbon, nitrogen, and phosphorus cycles resulting from plant-microbe interactions) are leading to these interactions increasingly being considered conservation priorities, while acute risks to their ecological and evolutionary persistence are being identified. The field of evolution came very late to the study of mutualism. Charles Darwin clearly recognized that it posed an evolutionary puzzle: In The Origin of Species, he wrote, “If it could be proved that any part of the structure of any one species had been formed for the exclusive good of another species, it would annihilate my theory, for such could not have been produced through natural selection.” The past 150 years have been devoted to trying to solve the challenge that Darwin posed to us.

General and Classic Works

It took a very long time for mutualism to be recognized as a concept—that is, as a biological phenomenon united by common features. In contrast, symbiosis, intimate interactions that can range from mutualistic to antagonistic, was recognized as a unified phenomenon very early, and a large literature accumulated about its origins and subsequent evolution. The study of symbiosis is given a thorough historical treatment in Sapp 1994 and is addressed in greater detail in the section Evolution of Symbiotic Mutualisms. The same broad perspective did not hold among researchers studying nonsymbiotic mutualisms. The vast majority of the earlier literature on these mutualisms centered on a single type of interaction. Pollination, long a focus in ecology and agricultural science, was of particular interest in an evolutionary context. Indeed, the only book Darwin devoted to evolution in an interspecific interaction, Darwin 1877, focused on insect pollination of orchids. A much later but highly influential treatment of the evolution of pollination was presented in Grant and Grant 1965. Daniel Janzen’s work on obligate ant-plant mutualisms, represented here in Janzen 1966, was critical in showing how field observations and experiments could be interpreted to illuminate the evolution of species interactions. Janzen’s studies also played an outsized role in making mutualisms a centerpiece of the study of coevolution. One of the earliest models of mutualism evolution was presented in Roughgarden 1975; while it dealt specifically with one marine mutualism, its generality was not lost on researchers. Modern interest in the evolution of cooperation as a whole, including but not restricted to cooperation between species, dates from Axelrod and Hamilton 1981, a towering contribution that posed the question of why cooperation should exist at all if organisms are under selection to act in their own best interests. The evolution of the eukaryotic cell is widely considered to have passed through a symbiotic stage. The classic reference on this topic (which lies outside the scope of this entry) is Margulis 1970. The breadth of modern concerns surrounding the evolution of mutualism is covered in Bronstein 2015, an edited volume whose individual chapters are cited in several of the sections below. Two valuable general chapters are the contributions Akcay 2015, an overview of theoretical approaches available to address questions surrounding mutualism evolution, and Baskett and Schemske 2015, covering the evolutionary genetics of mutualism.

• Akcay, E. 2015. Evolutionary models of mutualism. In Mutualism. Edited by J. L. Bronstein, 57–76. New York: Oxford Univ. Press.

  A unique, comprehensive, and accessible introduction to theoretical approaches currently used in studying mutualism evolution, as well as what they have revealed as of the early 21st century. Key topics include the origin and maintenance of mutualism, evolution of transmission mode, and control of cheaters.

• Axelrod, R., and W. D. Hamilton. 1981. The evolution of cooperation. Science 211.4489:1390–1396.

  DOI: 10.1126/science.7466396

  A conceptual contribution that launched the modern study of the evolution of all types of cooperation. Poses the question of when and why unrelated individuals should cooperate with each other, providing answers using a simple game theory model (tit-for-tat).

• Baskett, C. A., and D. W. Schemske. 2015. Evolution and genetics of mutualism. In Mutualism. Edited by J. L. Bronstein, 77–79. New York: Oxford Univ. Press.

  Comprehensive review of the genetic and genomic underpinnings of mutualism evolution. Starts from pollination, the best-understood mutualism from a genetic perspective, and extends to other, less heavily studied mutualisms. Highlights exciting directions for future investigation.

• Bronstein, J. L., ed. 2015. Mutualism. New York: Oxford Univ. Press.

  The only recent volume on mutualism as a unified phenomenon, and a useful entry for readers seeking a general introduction to the field. Several chapters address issues surrounding mutualism evolution. All chapters highlight open questions for future research.

• Darwin, C. 1877. On the various contrivances by which British and foreign orchids are fertilised by insects. 2d rev. ed. New York: D. Appleton.

  Darwin dove deep into understanding orchid adaptations to attract pollinators and how pollinator movements on flowers lead to pollination. A pioneering demonstration of how empirical studies, including small-scale experiments, can illuminate evolutionary patterns and processes. Reprinted 1984 (Chicago: Univ. of Chicago Press).

• Grant, V., and K. Grant. 1965. Flower pollination in the phlox family. New York: Columbia Univ. Press.

  A trailblazing treatment of pollination in a single plant family, and explicitly evolutionary in its consideration of the origin and diversification of key traits, particularly adaptations to attract and reward pollinators. Verne and Karen Grant build a strong link among floral traits, life histories, and breeding systems. Takes a strongly plant-centric approach.

• Janzen, D. H. 1966. Co-evolution of mutualism between ants and acacias in Central America. Evolution 20.3:249–275.

  DOI: 10.2307/2406628

  The best-known of Janzen’s impactful contributions to the study of mutualism and equally of coevolution. Lays out a convincing case, using diverse forms of evidence, that obligate associations between ants and Central American acacia plants are mutually beneficial, and that this mutualism is a product of cycles of evolution.

• Margulis, L. 1970. Origin of eukaryotic cells. New Haven, CT: Yale Univ. Press.

  Lynn Margulis here lays out a blazingly original interpretation of how eukaryotic cells evolved, including the successive incorporation of bacteria, which may have been mutualistic symbionts, into cell physiology and function as mitochondria and chloroplasts.

• Roughgarden, J. 1975. Evolution of marine symbiosis—a simple cost-benefit model. Ecology 56.5:1201–1208.

  DOI: 10.2307/1936160

  An early, highly influential evolutionary model of a mutualism (the anemone-clownfish interaction). Frames the problem in terms of costs and benefits of the interaction to each partner, a perspective that only much later was adopted in empirical studies of mutualism.

• Sapp, J. 1994. Evolution by association: A history of symbiosis. New York: Oxford Univ. Press.

  A useful historical overview of the study of symbiosis, with a particular focus on early work on mutualism. Evolutionary issues are incorporated into the discussion.