- Email: [email protected]
Evolutionary biology of host–parasite relationships: reality meets models
NEWS & COMMENT the activities of soil microbes and invertebrates. However, patchiness of soil processes involving microbes and invertebrates is, in turn, affected by the patchiness of soil inputs, including those determined by plants, e.g. the distribution of leaf litter and dead roots as a source of carbon for the soil biota. Reduction to single cause–effect relationships ignores the suite of feedback loops (each one patterned in space and time) of the system as a whole and the natural tendency for self-organizing systems (e.g. any biological system) to produce highly developed patterns from the slightest deviation from uniformity in the environment6,7. The study of ecological heterogeneity might need to become the study of ecological self-organization. The third issue was the identification of appropriate null models for studies of the effects of heterogeneity. The null model (and experimental control) is usually assumed to be homogeneous resources, conditions or pressures. However, this might not be logical. As Levin2 pointed out, all organisms, populations and ecosystems show heterogeneity and thus all should have been selected, in terms of physiological, morphological and demographic responses, for heterogeneity. When exposed to a new, homogeneous
environment, we should see a reduced functional response – exactly as illustrated convincingly in many case studies. Mark Rees (Imperial College, Silwood Park, UK) clearly demonstrated that biological systems will already be selected for heterogeneity. Comparison of four models of the flowering phenology of two monocarpic plant species from different environments (each model incorporating different types of heterogeneity in space and time) showed that observed times of flowering were affected by some, but not all, types of heterogeneity tested, and that the significant types of heterogeneity differed between the two species. Rees’ analysis represents a step beyond a simple comparison of heterogeneity and homogeneity, and raised the possibility that our thinking in the future might be about the ecological consequences of changes in the degree of environmental heterogeneity. There might still be some distance to go to achieve the theory of heterogeneity to which Steward Pickett aspires, but this symposium was an important station on the road. The gathering together of a heterogeneous group of ecologists to discuss ‘heterogeneity’ provided a timely multiscale synthesis of our progress and highlighted some important issues that might act as foci to guide future work.
Evolutionary biology of host–parasite relationships: reality meets models
P
arasites have adapted to treat almost every aspect of a free-living organism as a niche to exploit for their own benefit. Because parasitism is often harmful to the host, there is strong selective pressure on hosts to avoid or to be resistant to parasites. The resulting coevolutionary arms race is one of the most fascinating topics in evolutionary biology1,2. Moreover, the implications for public health and the economy, including such issues as drug resistance, make the understanding of host–parasite evolution vitally important. A recent workshop (3–7 May 1999) at the Laboratoire Arago in Banyuls-sur-Mer, France presented the latest advances in host–parasite evolutionary biology*. Oral contributions spanned the entire spectrum from empirical studies to applied mathematics. A round-table discussion *Poulin, R., Morand, S. and Skorping, A., eds Evolutionary Biology of Host–Parasite Relationships: Theory Meets Reality, Elsevier Science – due to be published in 2000. TREE vol. 14, no. 11 November 1999
addressed the crucial theoretical and empirical issues that will determine the future directions of the field.
Unsupported assumptions in models It is fundamentally important to have good empirical support for the assumptions upon which models are based, because these assumptions strongly influence experimental design and the significance of the results. Nevertheless, many participants agreed that there are several common assumptions that require more direct evidence. For instance, the level of parasite virulence is widely accepted to be the result of a trade-off between parasite transmission rate and host (and therefore parasite) mortality. However, experiments reported by Margaret Mackinnon (University of Edinburgh, UK) on mouse malaria (Plasmodium chabaudi) suggest that virulence is associated with a higher within-host replication rate, but found no evidence that increased host mortality by virulent strains selects for lower virulence. In general, trade-offs
Acknowledgements Mike Hutchings, Alan Stewart and Laurie Greenfield made valuable comments on an early draft. I would also like to thank the many other participants whose ideas contributed to this article, but who I could not include in detail.
Ashley D. Sparrow Dept of Plant and Microbial Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand ([email protected])
References 1 Chesson, P.L. and Case, T.J. (1986) Overview: non-equilibrium community theories: chance variability, history and coexistence, in Community Ecology (Diamond, J. and Case, T.J., eds), Harper and Row 2 Levin, S.A. (1992) The problem of pattern and scale in ecology, Ecology 73, 1943–1967 3 von Humboldt, A. and Bonpland, A. (1805) Essai sur la geographie des plantes, Levrault, Schoell et Cie 4 Watt, A.S. (1947) Pattern and process in the plant community, J. Ecol. 35, 1–22 5 Carroll, L. (1872) Through the Looking Glass and What Alice Found There, Macmillan 6 Kauffman, S.A. (1993) The Origins of Order: Selforganization and Selection in Evolution, Oxford University Press 7 Rohani, P. et al. (1997) Spatial selforganization in ecology: pretty patterns or robust reality? Trends Ecol. Evol. 12, 70–74
govern our thinking about host–parasite relationships, yet they are backed by little evidence. For example, Dag Atle Lysne (University of Tromsø, Norway) has tested the common prediction that resistance can have fitness costs, but was unable to detect any. Some participants were concerned about the almost ubiquitous use of deterministic models, of the Anderson and May type3, in modelling the population dynamics of parasite transmission. This approach is not always appropriate. For example, stochastic effects might be important in the population dynamics of some systems. Analyses of childhood disease dynamics presented by Bryan Grenfell (University of Cambridge, UK) demonstrate that stochastic corrections to a deterministic backbone model lead to a remarkable agreement with the data. However, this begs the question: when analysing real data, can one distinguish demographic stochasticity from measurement error? Theoretical studies suggest that, in certain nonlinear systems, the importance of demographic stochasticity can be inferred because it gives rise to phenomena not present in deterministic models. This was demonstrated by Stephen Cornell (University of Cambridge), who showed that demographic stochasticity
0169-5347/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved.
PII: S0169-5347(99)01727-9
423
NEWS & COMMENT in sexually reproducing macroparasites can lead to strong, systematic deviations from deterministic behaviour.
Empirical studies The difficulty of obtaining funding for long-term studies, and the resulting paucity of data, is unfortunate because some basic processes only occur over larger time scales, including speciation, species invasions and/or species dispersal, rare stochastic events (potentially causing inclusive random and hard selection), population cycles and even seasonal or longterm climatic changes. Long-term host– parasite field studies have yielded very rewarding data in the past; for example, Hudson et al.4 showed that parasites can destabilize host population dynamics. Many parasites reside inside their hosts. Often the damage caused, the mechanisms of the host–parasite interaction, and even the number of parasites can be determined only after sacrificing the host for dissection. This dramatically limits the number and types of study that can be conducted. This is especially true in long-term field studies, where repeated destructive sampling can significantly affect population sizes. The development of non-destructive sampling techniques is therefore desirable. To this end, Christine Müller-Graf (Université Pierre et Marie Curie, Paris, France) demonstrated that parasite egg counts in the host’s faeces can be reliably used to indicate which macroparasites infect vertebrate hosts, but cautioned that the correlation between egg counts and parasite numbers is unknown. The development of immunoassays should have similar benefits.
Comparative analysis Because comparative methods permit the meta-analysis of existing data, they have become widely used. Many participants felt that this popularity has been accompanied by abuse of the methods. For instance, it is imperative to analyse appropriate life-history traits, and these should not be subject to intraspecific (or interpopulational) variation. Another concern is that accurate phylogenies are essential to the comparative method, as this method controls for the effect of relatedness5. However, Andrea Simkova (Comenius University, Bratislava, Slovak Republic) showed that, in some instances, random phylogenies can be used to test for the sensitivity to phylogenetic correction. The power of comparative analyses lies in their ability to uncover broad correlations across taxa. The correlations produced by comparative analyses can be used to examine difficult issues that are not always amenable to experimentation. For example, Per Arneberg (University of
424
Tromsø, Norway) used the comparative method to reveal the factors determining population density in nematodes parasitizing mammals, highlighting the influence of host population density and betweenhost transmission on parasite abundance. Serge Morand (Université de Perpignan, France) also discussed how these methods can help our understanding of what determines parasite species richness in hosts. If used properly, comparative analyses hold great promise in examining correlations between numerous variables. Some participants also felt that the introduction of population genetic theories and approaches to among-species comparative analyses could enhance the use of comparative analyses further.
New theories Theory and models can be useful in proposing new and fruitful avenues of research, and in devising methods for testing basic hypotheses. However, care should be taken when applying general theories to specific problems, and models should be constructed with a particular system and question in mind. The empiricists at the workshop expressed a desire for more concrete and testable theories. More theoretical work on the coevolution of host–parasite variation is needed. The Red Queen model predicts that sexual reproduction can be used to generate variation that is useful in escaping parasitism. Sandrine Trouvé (Université de Lausanne, Switzerland) tested this prediction by sampling field populations of freshwater snails (Lymnaea truncatula), but did not find any correlation between parasite prevalence and host genetic diversity. Conversely, parasites can also sexually reproduce, mutate, or migrate to outmanoeuvre host defenses or find new susceptible hosts. Further, Dan Haydon (University of Edinburgh) suggested that the high mutation rate of some viruses does exactly that, generating temporarily unrecognizable new mutants. Theoretical advances are still necessary to understand the mechanistic constraints of host–parasite coevolutionary dynamics. For example, Armand Kuris (University of California, Santa Barbara, USA) proposed that host–parasite body size ratios are narrowly restricted and that, within the overall range, specific relationships are also narrowly defined. The physiological mechanisms that hosts use to achieve resistance to their parasites are also predicted to be costly6, limiting the host’s response to selection by parasites. Mark Rigby (ETH Zürich, Switzerland) presented a graphical model suggesting that resistance mechanisms
have life history costs under specific conditions. In an experimental test of this model, Yannick Moret (ETH Zürich) demonstrated the trade-off between resistance mechanisms and somatic maintenance. Game theory, population genetics and population dynamics are essential components of evolutionary theory, and the accurate modelling of complex host– parasite interactions might require a combination of these approaches. Jakob Koella (Université Pierre et Marie Curie, Paris, France) showed that optimization and population dynamic models can be successfully coupled to predict changes in host and parasite life histories. Population dynamic models predict, with empirical support, that parasites increase fluctuations in host population sizes4,7. Conversely, food-web models, working on the community scale, predict that the multiple, weak trophic interactions of parasites might dampen such fluctuations8,9. Can these two approaches be reconciled?
Prospects It could be argued that the workshop raised more questions than it answered. However, these questions suggest that host–parasite evolutionary biology is still a dynamic field with many productive areas of research remaining to be explored. One promising future avenue of research is the integration of several modelling techniques, such as population dynamics, population genetics, game theory and comparative methods. Another exciting future direction is the integration of the effects of multiple parasite species into models and experiments examining host–parasite interactions and coevolution. Coevolution, in turn, is fuelled by genetic variation in both hosts and parasites. The influence of mating systems, migration and mutation on genetic variation and, therefore, the rate and direction of the coevolutionary process, is an exciting new area of research just beginning to emerge. These new approaches and directions should lead to a greater understanding of the intrinsically complex nature of host–parasite evolutionary biology. Acknowledgements We would like to thank Dag Atle Lysne and Pej Rohani for discussions and comments. The workshop was organized by Serge Morand (Université de Perpignan, France), Robert Poulin (University of Otago, Dunedin, New Zealand) and Arne Skorping (University of Bergen, Norway), and was funded by the European Science Foundation, Centre National de la Recherche Scientifique, the Université de Perpignan, the Pôle Européen, and the Région Languedoc-Rousillon. TREE vol. 14, no. 11 November 1999
NEWS & COMMENT Stephen J. Cornell
Mark C. Rigby
Dept of Zoology, University of Cambridge, Downing Street, Cambridge, UK CB2 3EJ ([email protected])
ETH Zürich, Experimental Ecology, ETH Zentrum NW, CH-8092 Zürich, Switzerland ([email protected])
References Yves Desdevises Centre de Biologie et d’Écologie Tropicale et Méditerranéenne, Université de Perpignan, 66860 Perpignan, France; and Université de Montreal, Département de Sciences Biologiques, Montréal, Quebec, Canada H3C 3J7 ([email protected])
1 Ebert, D. and Hamilton, W.D. (1996) Sex against virulence: the coevolution of parasitic diseases, Trends Ecol. Evol. 11, 79–82 2 Thompson, J.N. (1994) The Coevolutionary Process, University of Chicago Press 3 Anderson, R.M. and May, R.M. (1991) Infectious Diseases of Humans, Oxford University Press 4 Hudson, P.J., Dobson, A.P. and Newborn, D. (1998) Prevention of population cycles by parasite removal, Science 282, 2256–2258
Driving sexual preference
O
ne of the oddest reports last year drew a connection between female mate choice and meiotic drive1. Several stalkeyed fly species show extreme eye-stalk dimorphism associated with strong female mate preferences for males with exaggerated eyespans. These species also have strongly female-biased sex ratios in the wild, which are caused by X-linked meiotic drive. Males carrying the Xd drive chromosome produce female-biased or femaleonly broods, because sperm carrying the Y chromosome degenerate2 (Box 1). Because the natural frequency of Xd is high, there is a female-biased population sex ratio. By contrast, all the sexually monomorphic species examined lack evidence of meiotic drive and have 1:1 sex ratios. But how has meiotic drive contributed to sexual selection? Wilkinson and colleagues suggested that the genes involved in meiotic drive were linked to those affecting male eyespan1. The first hint of this connection came as a fortuitous outcome of an artificial selection experiment on male eyespan. Several generations of selection on eyespan caused large correlated changes in sex ratio. In both lines selected for long eyespans (high lines), the sex ratio became more male-biased and approached 1:1 (the stock population is female-biased), whereas in one of the low lines the sex ratio became even more strongly female-biased. Wilkinson’s initial analysis indicated that these effects were Y-linked1. Previous work demonstrated the presence of Y-linked suppressors of drive (Ym)2, and their spread was thought to explain the 1:1 sex ratio in the high lines1. But, more recent work using backcrosses of the high lines to the controls failed to find TREE vol. 14, no. 11 November 1999
any evidence of Y-linked eyespan genes; instead, they implicated the X chromosome as having a major effect on male eyespan3. In addition, the more extreme female-bias in one of the low lines now appears to be a result of an increase in frequency of the Xd drive chromosome3. To date, the role of X or Y linkage has not been fully resolved. Understanding remains tentative, largely because markers do not exist for the Xd or Ym chromosomes, and their presence has to be inferred from brood sex ratios. Nonetheless, changes in eyespan are accompanied by changes in sex ratio, and this linkage needs to be explained.
Female preference for Y m suppressors Wilkinson’s observations suggest that male eyespan acts as an indicator of the suppression or absence of meiotic drive. This hypothesis has intuitive appeal because females benefit by producing a more even (or male-biased) sex ratio in a female-biased population4. Because males
5 Harvey, P.H. and Pagel, M.D. (1991) The Comparative Method in Evolutionary Biology, Oxford University Press 6 Sheldon, B.C. and Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology, Trends Ecol. Evol. 11, 317–321 7 May, R.M. (1973) Complexity and Stability of Model Ecosystems, Princeton University Press 8 McCann, K., Hastings, A. and Huxel, G.R. (1998) Weak trophic interactions and the balance of nature, Nature 395, 794–798 9 Freeland, W.J. and Boulton, W.J. (1992) Coevolution of food webs: parasites, predators, and plant secondary compounds, Biotropica 24, 309–327
are rare, they have a higher mean reproductive value than females; therefore, a female mating with a male without meiotic drive (either suppressed or absent) will be fitter because she leaves a greater number of grandchildren. Maybe this could explain the evolution of female preference for large male eyespan in sexually dimorphic species1,5. Two new theoretical papers have now examined whether such a process is possible3,6. Reinhold et al.6 consider female choice for Ym. They studied a population genetic model of meiotic drive, which simulates the evolution of Xd meiotic drive and Ym suppression of drive. Under standard assumptions, the model predicts evolution to a polymorphic equilibrium, as seen in stalk-eyed flies1,2. However, against intuition, the model shows that female choice for Ym is always deleterious. Imagine Ym is linked to a gene for male long eyespan. Females choosing long eyespan males appear to benefit, because these males suppress meiotic drive if they carry the Xd chromosome, and so always produce an equal number of male and female offspring. By contrast, short eyespan males lack the Y suppressor and produce female-biased broods if they carry the Xd chromosome.
Box 1. Meiotic drive X-linked meiotic drive is known in a number of Diptera, mainly Drosophila8,9. In stalk-eyed flies, XdY males produce normal Xd sperm and degenerate Y sperm2. Consequently, brood sex ratios are heavily femalebiased. Xd is an example of a selfish genetic element, which spreads because it increases its transmission rate to the next generation. However, this is costly to the rest of the genome because half the sperm are lost, the sex ratio of offspring is distorted, and in several Drosophila species, Xd reduces female viability. These deleterious effects stop Xd from spreading to fixation. Y-linked suppressors of meiotic drive are known in several species8,9. In stalk-eyed flies, the Ym suppressor is immune to the action of Xd. Ym sperm no longer appear degenerate in XdYm males, and the brood sex ratio is even2. In fact, there is a slight male-bias in offspring of XdYm males, which might be caused by slight Xd sperm dysfunction2. The Ym chromosome is polymorphic in populations of stalk-eyed flies, which suggests that it is costly2, although this has not been formally demonstrated. If drive suppression is costly, Ym will spread when drive is common but will be selected against when drive is rare. The net effect will keep both the drive and suppressor loci polymorphic.
0169-5347/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(99)01701-2
425
environment, we should see a reduced functional response – exactly as illustrated convincingly in many case studies. Mark Rees (Imperial College, Silwood Park, UK) clearly demonstrated that biological systems will already be selected for heterogeneity. Comparison of four models of the flowering phenology of two monocarpic plant species from different environments (each model incorporating different types of heterogeneity in space and time) showed that observed times of flowering were affected by some, but not all, types of heterogeneity tested, and that the significant types of heterogeneity differed between the two species. Rees’ analysis represents a step beyond a simple comparison of heterogeneity and homogeneity, and raised the possibility that our thinking in the future might be about the ecological consequences of changes in the degree of environmental heterogeneity. There might still be some distance to go to achieve the theory of heterogeneity to which Steward Pickett aspires, but this symposium was an important station on the road. The gathering together of a heterogeneous group of ecologists to discuss ‘heterogeneity’ provided a timely multiscale synthesis of our progress and highlighted some important issues that might act as foci to guide future work.
Evolutionary biology of host–parasite relationships: reality meets models
P
arasites have adapted to treat almost every aspect of a free-living organism as a niche to exploit for their own benefit. Because parasitism is often harmful to the host, there is strong selective pressure on hosts to avoid or to be resistant to parasites. The resulting coevolutionary arms race is one of the most fascinating topics in evolutionary biology1,2. Moreover, the implications for public health and the economy, including such issues as drug resistance, make the understanding of host–parasite evolution vitally important. A recent workshop (3–7 May 1999) at the Laboratoire Arago in Banyuls-sur-Mer, France presented the latest advances in host–parasite evolutionary biology*. Oral contributions spanned the entire spectrum from empirical studies to applied mathematics. A round-table discussion *Poulin, R., Morand, S. and Skorping, A., eds Evolutionary Biology of Host–Parasite Relationships: Theory Meets Reality, Elsevier Science – due to be published in 2000. TREE vol. 14, no. 11 November 1999
addressed the crucial theoretical and empirical issues that will determine the future directions of the field.
Unsupported assumptions in models It is fundamentally important to have good empirical support for the assumptions upon which models are based, because these assumptions strongly influence experimental design and the significance of the results. Nevertheless, many participants agreed that there are several common assumptions that require more direct evidence. For instance, the level of parasite virulence is widely accepted to be the result of a trade-off between parasite transmission rate and host (and therefore parasite) mortality. However, experiments reported by Margaret Mackinnon (University of Edinburgh, UK) on mouse malaria (Plasmodium chabaudi) suggest that virulence is associated with a higher within-host replication rate, but found no evidence that increased host mortality by virulent strains selects for lower virulence. In general, trade-offs
Acknowledgements Mike Hutchings, Alan Stewart and Laurie Greenfield made valuable comments on an early draft. I would also like to thank the many other participants whose ideas contributed to this article, but who I could not include in detail.
Ashley D. Sparrow Dept of Plant and Microbial Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand ([email protected])
References 1 Chesson, P.L. and Case, T.J. (1986) Overview: non-equilibrium community theories: chance variability, history and coexistence, in Community Ecology (Diamond, J. and Case, T.J., eds), Harper and Row 2 Levin, S.A. (1992) The problem of pattern and scale in ecology, Ecology 73, 1943–1967 3 von Humboldt, A. and Bonpland, A. (1805) Essai sur la geographie des plantes, Levrault, Schoell et Cie 4 Watt, A.S. (1947) Pattern and process in the plant community, J. Ecol. 35, 1–22 5 Carroll, L. (1872) Through the Looking Glass and What Alice Found There, Macmillan 6 Kauffman, S.A. (1993) The Origins of Order: Selforganization and Selection in Evolution, Oxford University Press 7 Rohani, P. et al. (1997) Spatial selforganization in ecology: pretty patterns or robust reality? Trends Ecol. Evol. 12, 70–74
govern our thinking about host–parasite relationships, yet they are backed by little evidence. For example, Dag Atle Lysne (University of Tromsø, Norway) has tested the common prediction that resistance can have fitness costs, but was unable to detect any. Some participants were concerned about the almost ubiquitous use of deterministic models, of the Anderson and May type3, in modelling the population dynamics of parasite transmission. This approach is not always appropriate. For example, stochastic effects might be important in the population dynamics of some systems. Analyses of childhood disease dynamics presented by Bryan Grenfell (University of Cambridge, UK) demonstrate that stochastic corrections to a deterministic backbone model lead to a remarkable agreement with the data. However, this begs the question: when analysing real data, can one distinguish demographic stochasticity from measurement error? Theoretical studies suggest that, in certain nonlinear systems, the importance of demographic stochasticity can be inferred because it gives rise to phenomena not present in deterministic models. This was demonstrated by Stephen Cornell (University of Cambridge), who showed that demographic stochasticity
0169-5347/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved.
PII: S0169-5347(99)01727-9
423
NEWS & COMMENT in sexually reproducing macroparasites can lead to strong, systematic deviations from deterministic behaviour.
Empirical studies The difficulty of obtaining funding for long-term studies, and the resulting paucity of data, is unfortunate because some basic processes only occur over larger time scales, including speciation, species invasions and/or species dispersal, rare stochastic events (potentially causing inclusive random and hard selection), population cycles and even seasonal or longterm climatic changes. Long-term host– parasite field studies have yielded very rewarding data in the past; for example, Hudson et al.4 showed that parasites can destabilize host population dynamics. Many parasites reside inside their hosts. Often the damage caused, the mechanisms of the host–parasite interaction, and even the number of parasites can be determined only after sacrificing the host for dissection. This dramatically limits the number and types of study that can be conducted. This is especially true in long-term field studies, where repeated destructive sampling can significantly affect population sizes. The development of non-destructive sampling techniques is therefore desirable. To this end, Christine Müller-Graf (Université Pierre et Marie Curie, Paris, France) demonstrated that parasite egg counts in the host’s faeces can be reliably used to indicate which macroparasites infect vertebrate hosts, but cautioned that the correlation between egg counts and parasite numbers is unknown. The development of immunoassays should have similar benefits.
Comparative analysis Because comparative methods permit the meta-analysis of existing data, they have become widely used. Many participants felt that this popularity has been accompanied by abuse of the methods. For instance, it is imperative to analyse appropriate life-history traits, and these should not be subject to intraspecific (or interpopulational) variation. Another concern is that accurate phylogenies are essential to the comparative method, as this method controls for the effect of relatedness5. However, Andrea Simkova (Comenius University, Bratislava, Slovak Republic) showed that, in some instances, random phylogenies can be used to test for the sensitivity to phylogenetic correction. The power of comparative analyses lies in their ability to uncover broad correlations across taxa. The correlations produced by comparative analyses can be used to examine difficult issues that are not always amenable to experimentation. For example, Per Arneberg (University of
424
Tromsø, Norway) used the comparative method to reveal the factors determining population density in nematodes parasitizing mammals, highlighting the influence of host population density and betweenhost transmission on parasite abundance. Serge Morand (Université de Perpignan, France) also discussed how these methods can help our understanding of what determines parasite species richness in hosts. If used properly, comparative analyses hold great promise in examining correlations between numerous variables. Some participants also felt that the introduction of population genetic theories and approaches to among-species comparative analyses could enhance the use of comparative analyses further.
New theories Theory and models can be useful in proposing new and fruitful avenues of research, and in devising methods for testing basic hypotheses. However, care should be taken when applying general theories to specific problems, and models should be constructed with a particular system and question in mind. The empiricists at the workshop expressed a desire for more concrete and testable theories. More theoretical work on the coevolution of host–parasite variation is needed. The Red Queen model predicts that sexual reproduction can be used to generate variation that is useful in escaping parasitism. Sandrine Trouvé (Université de Lausanne, Switzerland) tested this prediction by sampling field populations of freshwater snails (Lymnaea truncatula), but did not find any correlation between parasite prevalence and host genetic diversity. Conversely, parasites can also sexually reproduce, mutate, or migrate to outmanoeuvre host defenses or find new susceptible hosts. Further, Dan Haydon (University of Edinburgh) suggested that the high mutation rate of some viruses does exactly that, generating temporarily unrecognizable new mutants. Theoretical advances are still necessary to understand the mechanistic constraints of host–parasite coevolutionary dynamics. For example, Armand Kuris (University of California, Santa Barbara, USA) proposed that host–parasite body size ratios are narrowly restricted and that, within the overall range, specific relationships are also narrowly defined. The physiological mechanisms that hosts use to achieve resistance to their parasites are also predicted to be costly6, limiting the host’s response to selection by parasites. Mark Rigby (ETH Zürich, Switzerland) presented a graphical model suggesting that resistance mechanisms
have life history costs under specific conditions. In an experimental test of this model, Yannick Moret (ETH Zürich) demonstrated the trade-off between resistance mechanisms and somatic maintenance. Game theory, population genetics and population dynamics are essential components of evolutionary theory, and the accurate modelling of complex host– parasite interactions might require a combination of these approaches. Jakob Koella (Université Pierre et Marie Curie, Paris, France) showed that optimization and population dynamic models can be successfully coupled to predict changes in host and parasite life histories. Population dynamic models predict, with empirical support, that parasites increase fluctuations in host population sizes4,7. Conversely, food-web models, working on the community scale, predict that the multiple, weak trophic interactions of parasites might dampen such fluctuations8,9. Can these two approaches be reconciled?
Prospects It could be argued that the workshop raised more questions than it answered. However, these questions suggest that host–parasite evolutionary biology is still a dynamic field with many productive areas of research remaining to be explored. One promising future avenue of research is the integration of several modelling techniques, such as population dynamics, population genetics, game theory and comparative methods. Another exciting future direction is the integration of the effects of multiple parasite species into models and experiments examining host–parasite interactions and coevolution. Coevolution, in turn, is fuelled by genetic variation in both hosts and parasites. The influence of mating systems, migration and mutation on genetic variation and, therefore, the rate and direction of the coevolutionary process, is an exciting new area of research just beginning to emerge. These new approaches and directions should lead to a greater understanding of the intrinsically complex nature of host–parasite evolutionary biology. Acknowledgements We would like to thank Dag Atle Lysne and Pej Rohani for discussions and comments. The workshop was organized by Serge Morand (Université de Perpignan, France), Robert Poulin (University of Otago, Dunedin, New Zealand) and Arne Skorping (University of Bergen, Norway), and was funded by the European Science Foundation, Centre National de la Recherche Scientifique, the Université de Perpignan, the Pôle Européen, and the Région Languedoc-Rousillon. TREE vol. 14, no. 11 November 1999
NEWS & COMMENT Stephen J. Cornell
Mark C. Rigby
Dept of Zoology, University of Cambridge, Downing Street, Cambridge, UK CB2 3EJ ([email protected])
ETH Zürich, Experimental Ecology, ETH Zentrum NW, CH-8092 Zürich, Switzerland ([email protected])
References Yves Desdevises Centre de Biologie et d’Écologie Tropicale et Méditerranéenne, Université de Perpignan, 66860 Perpignan, France; and Université de Montreal, Département de Sciences Biologiques, Montréal, Quebec, Canada H3C 3J7 ([email protected])
1 Ebert, D. and Hamilton, W.D. (1996) Sex against virulence: the coevolution of parasitic diseases, Trends Ecol. Evol. 11, 79–82 2 Thompson, J.N. (1994) The Coevolutionary Process, University of Chicago Press 3 Anderson, R.M. and May, R.M. (1991) Infectious Diseases of Humans, Oxford University Press 4 Hudson, P.J., Dobson, A.P. and Newborn, D. (1998) Prevention of population cycles by parasite removal, Science 282, 2256–2258
Driving sexual preference
O
ne of the oddest reports last year drew a connection between female mate choice and meiotic drive1. Several stalkeyed fly species show extreme eye-stalk dimorphism associated with strong female mate preferences for males with exaggerated eyespans. These species also have strongly female-biased sex ratios in the wild, which are caused by X-linked meiotic drive. Males carrying the Xd drive chromosome produce female-biased or femaleonly broods, because sperm carrying the Y chromosome degenerate2 (Box 1). Because the natural frequency of Xd is high, there is a female-biased population sex ratio. By contrast, all the sexually monomorphic species examined lack evidence of meiotic drive and have 1:1 sex ratios. But how has meiotic drive contributed to sexual selection? Wilkinson and colleagues suggested that the genes involved in meiotic drive were linked to those affecting male eyespan1. The first hint of this connection came as a fortuitous outcome of an artificial selection experiment on male eyespan. Several generations of selection on eyespan caused large correlated changes in sex ratio. In both lines selected for long eyespans (high lines), the sex ratio became more male-biased and approached 1:1 (the stock population is female-biased), whereas in one of the low lines the sex ratio became even more strongly female-biased. Wilkinson’s initial analysis indicated that these effects were Y-linked1. Previous work demonstrated the presence of Y-linked suppressors of drive (Ym)2, and their spread was thought to explain the 1:1 sex ratio in the high lines1. But, more recent work using backcrosses of the high lines to the controls failed to find TREE vol. 14, no. 11 November 1999
any evidence of Y-linked eyespan genes; instead, they implicated the X chromosome as having a major effect on male eyespan3. In addition, the more extreme female-bias in one of the low lines now appears to be a result of an increase in frequency of the Xd drive chromosome3. To date, the role of X or Y linkage has not been fully resolved. Understanding remains tentative, largely because markers do not exist for the Xd or Ym chromosomes, and their presence has to be inferred from brood sex ratios. Nonetheless, changes in eyespan are accompanied by changes in sex ratio, and this linkage needs to be explained.
Female preference for Y m suppressors Wilkinson’s observations suggest that male eyespan acts as an indicator of the suppression or absence of meiotic drive. This hypothesis has intuitive appeal because females benefit by producing a more even (or male-biased) sex ratio in a female-biased population4. Because males
5 Harvey, P.H. and Pagel, M.D. (1991) The Comparative Method in Evolutionary Biology, Oxford University Press 6 Sheldon, B.C. and Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology, Trends Ecol. Evol. 11, 317–321 7 May, R.M. (1973) Complexity and Stability of Model Ecosystems, Princeton University Press 8 McCann, K., Hastings, A. and Huxel, G.R. (1998) Weak trophic interactions and the balance of nature, Nature 395, 794–798 9 Freeland, W.J. and Boulton, W.J. (1992) Coevolution of food webs: parasites, predators, and plant secondary compounds, Biotropica 24, 309–327
are rare, they have a higher mean reproductive value than females; therefore, a female mating with a male without meiotic drive (either suppressed or absent) will be fitter because she leaves a greater number of grandchildren. Maybe this could explain the evolution of female preference for large male eyespan in sexually dimorphic species1,5. Two new theoretical papers have now examined whether such a process is possible3,6. Reinhold et al.6 consider female choice for Ym. They studied a population genetic model of meiotic drive, which simulates the evolution of Xd meiotic drive and Ym suppression of drive. Under standard assumptions, the model predicts evolution to a polymorphic equilibrium, as seen in stalk-eyed flies1,2. However, against intuition, the model shows that female choice for Ym is always deleterious. Imagine Ym is linked to a gene for male long eyespan. Females choosing long eyespan males appear to benefit, because these males suppress meiotic drive if they carry the Xd chromosome, and so always produce an equal number of male and female offspring. By contrast, short eyespan males lack the Y suppressor and produce female-biased broods if they carry the Xd chromosome.
Box 1. Meiotic drive X-linked meiotic drive is known in a number of Diptera, mainly Drosophila8,9. In stalk-eyed flies, XdY males produce normal Xd sperm and degenerate Y sperm2. Consequently, brood sex ratios are heavily femalebiased. Xd is an example of a selfish genetic element, which spreads because it increases its transmission rate to the next generation. However, this is costly to the rest of the genome because half the sperm are lost, the sex ratio of offspring is distorted, and in several Drosophila species, Xd reduces female viability. These deleterious effects stop Xd from spreading to fixation. Y-linked suppressors of meiotic drive are known in several species8,9. In stalk-eyed flies, the Ym suppressor is immune to the action of Xd. Ym sperm no longer appear degenerate in XdYm males, and the brood sex ratio is even2. In fact, there is a slight male-bias in offspring of XdYm males, which might be caused by slight Xd sperm dysfunction2. The Ym chromosome is polymorphic in populations of stalk-eyed flies, which suggests that it is costly2, although this has not been formally demonstrated. If drive suppression is costly, Ym will spread when drive is common but will be selected against when drive is rare. The net effect will keep both the drive and suppressor loci polymorphic.
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