© 2002 by The Society for Integrative and Comparative Biology
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Themes from Variation: Probing the Commonalities of Symbiotic Associations1
1 Department of Life Sciences, Arizona State University West, P.O. Box 37100 Phoenix, Arizona 85069-7100
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Research on symbiosis (including antagonistic and mutualistic associations) wrestles, directly or indirectly, with the paradox: why are symbiotic associations so prevalent in the biosphere in the face of ubiquitous immune or antibiotic defenses among organisms? The symposium "Living Together: the Dynamics of Symbiotic Interactions" considered several questions: 1. How do symbiotic species partners come together? Do symbioses share similar patterns of signal recognition and response? 2. What roles do nutrients and metabolites play in symbiotic interactions, and how are metabolic exchanges affected by environmental changes? 3. In what ways do the dynamics of multispecies symbioses differ from two-species associations? 4. How do antagonistic (parasitic, pathogenic) symbioses differ from mutualistic ones? In what ways do changes in the biotic and physical environment affect the evolutionary balance of symbiotic associations? 5. What are the coevolutionary patterns of symbiotic associations? 6. Which research techniques, and strategies of experimental design, might be useful across a broad range of symbiotic associations?
Two themes emerged from the symposium. First, all the participants have incorporated multiple techniques and perspectives into their work, approaches which facilitate the understanding of symbiotic dynamics at several levels of biological organization. Secondly, many of the papers addressed genetic and environmental variation in symbiotic interactions. Such approaches are useful tools for analysis of the mechanics of interspecies interactions and for characterization of the most important factors which influence them. They provide us with the tools to evaluate symbioses in a world of complexity, variation and change.
Nothing unconnected ever occurs.—sign on a church, Cambridge, Massachusetts
So essential is the property of self/non-self recognition to life, and so ingrained is the perspective that absence of infection is a requisite of organismal health, that symbiotic interactions (protracted, intimate associations between two or more species: Saffo, 1992b) continue to surprise us, even as we continue to document the ubiquitous distribution of symbioses in the biosphere. We are intrigued by these apparent exceptions to our axenic rule, by ways in which species can live for extended periods in close association with another—often inside another—despite immune defenses which should make such ways of life improbable or impossible.
Perhaps in part because of the diversity of these "exceptions," as well as the technical complexities of studying symbiotic interactions, researchers have tended to focus empirical work on individual symbioses, and on their implications for the particular taxa involved, or the ecological, evolutionary, nutritional, medical or agricultural relevance of each. There is no doubt that each symbiosis provides particular points of fascination, and each offers particular developmental, physiological, evolutionary or ecological lessons for us. Consider these few examples.
- Obligate symbionts often differ in striking ways from their free-living relatives, reflecting the special evolutionary challenges of symbiotic life.
• Among parasitic crustaceans, the "wonderfully grotesque" (Roberts and Janovy, 2000
) morphologies of adult females in several species of parasitic copepods and isopods differ so strongly from their free-living counterparts that their crustacean features are recognizable only to the specialist observer. As they invade decapod hosts, females of several species of parasitic barnacles lose all morphological traces of barnacle (indeed, of metazoan) organs and appendages, forming a fungus-like, invasive cellular mass within their crustacean hosts; organismal traces of their crustacean affinities remain only in the eventual production of bona fide barnacle larvae, and in their successful subversion of the reproductive physiology of their fellow crustacean hosts to serve their own reproductive needs (Høeg, 1985; Glenner and Høeg, 1995; Gould, 1996).
- The presence of endosymbionts can have striking effects on the morphology, behavior and ecology of hosts.
• Inter-host transmission is a perilous part of the life cycle for obligately symbiotic organisms, especially complicated among those who colonize, successively, two or more host taxa in the course of their life cycle. The solution of several apicomplexan, acanthocephalan and trematode parasites to this problem is a particularly efficient yet improbable one. They alter the behavior of their respective intermediate hosts, resulting in the movement of intermediate hosts, cum parasites, to unusually conspicuous, predator-accessible locations, thereby enhancing the probability of ingestion of the parasite-infected intermediate host by the next host in the parasite's life cycle (Berdoy et al., 2000; Curtis, 1987; Moore, 1984, 2002).
• Organs of several cephalopods and marine fish, colonized by luminous bacteria, provide extraordinary examples of the possibilities of coevolutionary innovation and coordination. The exquisite adaptation of such organs for maintenance of the bacterial symbionts and exploitation of bacterial luminescence by their animal hosts is evidenced not only by the structure of the light organs themselves, but by the intricate ways in which their function is enhanced and honed by nervous and environmental regulation; in pony fish (Leiognathus equulus; Hastings, 1971), this coordination extends even to other organs, by directed transmission of symbiotic light from the light organ through the swim bladder and neighboring tissues (Hastings, 1971; Morin et al., 1975; McFall-Ngai, 1991, 1999).
• Lichens are symbiotic associations of green algae (and/or cyanobacteria) and fungi (usually ascomycetes), but they are much more than the sum of their microbial parts. Morphological evidence for symbiotic synergy can be seen in foliose and fruticose lichens (about 20–25% of all lichens), where association of the microscopic algal and fungal symbionts yields a highly organized, macroscopic thallus resembling a single, multicellular organism (Indeed, lichens were thought to be such until 1867). So consistent are lichen forms that early biologists created workable lichen taxonomies treating a single lichen thallus as a systematic unit; despite their phylogenetic limitations, these traditional taxonomies are still used as practical systems for field identification. Lichen symbioses also show ecological synergy, thriving in often severe habitats where aposymbiotic algal or fungal partners rarely grow alone (Nash, 1996; Purvis, 2000).
- Symbiotic associations have had signficant evolutionary impact.
Symbiotic interactions are associated with a number of major evolutionary events, notably the evolution of eukaryotic organisms and the evolution of land plants. It is now generally accepted that at least two organelles central to eukaryote biology—mitochondria and chloroplasts—are of symbiotic ancestry (Gilham, 1994; Margulis, 1993; Margulis and Fester, 1991). The ancient and nearly-ubiquitous association of vascular plants with mycorrhizae (especially arbuscular mycorrhizae: Malloch et al., 1980, Smith and Read, 1997) suggests that mycorrhizal symbiosis has been closely bound up with the evolution and radiation of plants on land. Radiations of several metazoan taxa (vestimentiferan pogonophorans, molgulid tunicates, leiognathid fishes, sepiolid squid, aphids, among others: Margulis and Fester, 1991; McFall-Ngai, 1991, 1999; Moran and Telang, 1998; Nishiguchi et al., 1998, Moran and Baumann, 2000; Saffo, 1991a, b) have been shaped at least in part by coevolution with resident microbial endosymbionts.
- The products of many symbioses, and the effects of symbiosis on plant, animal and human hosts are of ecological, agricultural and medical importance.
• Human infections with eukaryotic parasites represent a major health problem; death rates from schistosomiasis and malaria alone are estimated (Roberts and Janovy, 2000; Su et al., 1995) at 1.5–3 million per year.
• The herbivorous habits of many mammals and insects, as well as other herbivorous animals, are strongly dependent on the metabolic activities of bacterial and protistan symbionts (Buchner, 1965; Breznak, 1982; Martin, 1991; Nardon and Grenier, 1991; Saffo, 1992a). Many of these animals—including especially domesticated ruminants—play key roles in agriculture.
• Shallow-water scleractinian corals are dependent on dinoflagellate symbionts for most of their carbon nutrition, for calcification, and, thus, also for reef-building. Through their net primary productivity and in providing a physical structure for tropical reef communities, dinoflagellate-scleractinian symbioses are central contributors to the productivity and community structure of reef ecosystems (Veron, 1995; Rowan and Knowlton, 1995; Rowan, 1998).
• The very wide distribution of arbuscular mycorrhizae and ectomycorrhizae among terrestrial plants is of enormous ecological and agricultural significance, especially in enhancement of phosphorus uptake and growth in plant hosts in low-phosphorus soils. Rhizobium-mediated nitrogen fixation among legumes is of similar ecological and agricultural importance (Saffo, 2001; Smith and Read, 1997).
- The presence of endosymbionts can have striking effects on the morphology, behavior and ecology of hosts.
It could be argued that the only shared feature of these sample symbioses is their diversity. They involve disparate taxonomic groups, and a wide range of habitats and ecosystems. Each symbiosis has distinct patterns of metabolic exchange, differing degrees of morphological and physiological intimacy, and differing evolutionary outcomes. Each of these poses a distinct set of experimental and technical challenges. Each of these varies in degree and kind of evolutionary and ecological significance.
But it is worth considering the general significance of symbiotic interactions, in addition to the smaller lessons of individual symbioses. However bizarre some symbiotic organisms may seem to us, the ubiquitous taxonomic and geographical distribution of symbioses (Saffo, 1991b, 2001) remind us that symbiotic associations are not oddities (truly axenic organisms are arguably the real oddities), but pervasive features of the biosphere. This pervasiveness raises the general paradox: why are symbiotic associations so common and how are they maintained in the face of ubiquitous immune and antibiotic defenses?
Other questions flow from this paradox. What series of genetic events accompany the sometimes profound morphological and physiological modifications of endosymbiotic organisms compared to free-living forms? Does evolution from free-living to symbiotic life proceed rapidly (Lutzoni and Pagel, 1997)? Is symbiosis reversible? Can free-living taxa arise from symbiotic ancestors, despite the specializations, modifications and dependencies characteristic of many symbiotic species (Hibbett et al., 2000; Moran and Wernegreen, 2000; Saffo, 1991b)? Does coevolution between symbiotic partners necessarily lead either to increasing host-symbiont specificity over evolutionary time, or to cospeciation? Do different kinds of symbioses share similarities in mechanisms of symbiont-host recognition—in chemical pathways, in cell-surface antigens or receptors, or in sequential patterns of signals between symbiont and host? In what ways do symbiotic associations interact with the environment, and how are they affected by both biotic (other interacting species, physiological condition of the symbiotic partners themselves) and physical aspects of the environment? Do coevolutionary patterns differ in obligate and facultative associations, among hereditary and horizontally transmitted symbioses? What genetic, physiological or ecological factors determine evolutionary outcome? Which environments seem to support particularly high incidences of mutualistic or antagonistic symbiosis? Do parasitic and mutualistic symbioses differ in patterns of coevolution?
The symposium, "Living Together: the Dynamics of Symbiotic Interactions," was organized to consider these kinds of questions. To maximize the breadth of dialogue, speakers were drawn from many fields of both basic and applied research—plant molecular biology, parasitology, plant ecology, mycology, microbiology, mammalian physiology, agricultural research, lichen systematics, marine paleobiology, coral reef ecology, evolutionary ecology of plant-insect interactions, malaria genetics, genetics and developmental biology of Drosophila, behavioral genetics and anti-viral computer technology. Of the 18 speakers, 14 papers are included in these published proceedings.
During the symposium, a number of recurring questions and themes arose. Some of these questions were included in the formal structure of the symposium; others emerged in the course of informal discussions during the meeting. Papers which relate to the particular topics of discussion are listed parenthetically, by author, at the end of each group of the following questions:
- a. How do symbiotic species partners come together? Do symbioses share similar patterns of signal recognition and response? Are there differences in responses of hosts to pathogenic and beneficial symbionts?
• (Lum et al., Esch et al., Bruns et al., Sorenson and Payne, Evans and Wellems)
- b. What kinds of nutrients and metabolites are produced and transported in symbiotic interactions, and what roles do these compounds play in symbioses? How are metabolic exchanges affected by changes in species partners, or by environmental changes?
• (Lum et al., Breznak, Mackie, Simpson et al., Bruns et al., Simms and Taylor)
- c. In what ways do the dynamics of multispecies symbioses differ from two-species associations? What are the similarities and differences between simultaneous multi-species associations, and sequential ones? Are there competitive or complementary interactions among symbionts in multi-species associations?
• (Lum et al., Esch et al., Breznak, Mackie, Simpson et al., Bruns et al., Simms and Taylor, Thompson et al.)
- d. How do antagonistic (parasitic, pathogenic) symbioses differ from mutualistic ones? Which factors favor the evolution of mutualists? Do mutualisms and parasitisms show different degrees of host specificity? In what ways do changes in the biotic and physical environment affect the evolutionary balance of symbiotic associations?
• (Lum et al., Simpson et al., Bruns et al., Faeth and Fagan, Simms and Taylor, Thompson et al., Sorenson and Payne, Evans and Wellems)
- e. What are the coevolutionary patterns of symbiotic associations? Can symbiosis serve as a mechanism for speciation? In obligate symbioses, does host specificity increase over evolutionary time? How do symbiotic associations spread through hosts populations? Do antagonistic symbioses become more benign over time? Is host specificity always correlated with cospeciation? Is specialization for symbiotic life an evolutionarily irreversible step?
• (Clark and Karr, Telschow et al., Thompson et al., Sorenson and Payne, Evans and Wellems)
- f. Which research techniques, and strategies of experimental design, might be useful across a broad range of symbiotic associations? Participants in the symposium recounted a number of techniques, all of which were used by at least several of the symbiosis researchers at the meeting:
1. field sampling and experimentation (Esch et al., Bruns et al., Faeth and Fagan, Thompson et al., Sorenson and Payne, Evans and Wellems)
2. modeling (Mackie, Telschow et al., Faeth and Fagan, Simms and Taylor, Thompson et al.)
3. molecular and cellular techniques (Lum et al., Breznak, Clark and Karr)
4. molecular genetics, molecular systematics (Breznak, Mackie, Simpson et al., Clark and Karr, Bruns et al., Faeth and Fagan, Sorenson and Payne, Evans and Wellems).
- b. What kinds of nutrients and metabolites are produced and transported in symbiotic interactions, and what roles do these compounds play in symbioses? How are metabolic exchanges affected by changes in species partners, or by environmental changes?
Two common themes have emerged among the symposium papers. First, as the above list suggests, all the authors have incorporated multiple techniques and perspectives in their work, integrating laboratory work with field or clinical data, empirical data with computer models, evolutionary perspectives with molecular, physiological and cellular data. A second theme, encouraged by the development of landscape ecology and by recent advances in sequencing technology, is an increased awareness of, and assessment of, genetic and environmental variation in symbiotic interactions. Both these themes are welcome trends. Integration of multiple techniques and perspectives facilitate the understanding of symbiotic dynamics at several levels of biological organization. Assessments of genetic and environmental variation in symbiosis dynamics are useful tools for characterizing the detailed mechanics of interspecies interactions and for defining the most important factors which influence them. More generally, they provide us with the tools to evaluate symbioses in the real world—that is, a world of complexity, genetic, physiological and environmental variation, and change.
As befits a field focused on interactions (Saffo, 1992b), the symposium encouraged symbiosis researchers to make new connections among fellow biologists from disparate fields, and to find commonalities among their diverse experimental systems. As a group of plant pathologists wrote recently (Cohn et al., 2001), "In the future, the sharing of ideas among plant and animal biologists is likely to broaden our understanding of defence responses in diverse organisms." So it is with all aspects of symbiotic interactions. We thank the SICB and the US Department of Agriculture (award # 2001-35204-10254) for providing the opportunity to share ideas and questions, to discuss common problems, and to discover common ground.
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1 From the Symposium Living Together: The Dynamics Of Symbiotic Interactions presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 Present address: Museum of Comparative Zoology Labs 408, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138; E-mail: mbsaffo{at}oeb.harvard.edu
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