- Email: [email protected]
Corals and phase shifts
126
News & Comment
TRENDS in Ecology & Evolution Vol.16 No.3 March 2001
Letters
Dear Mr Darwin: Help! Comment from Dover
I wrote a book called Dear Mr Darwin1. Brian Charlesworth has written a review2 of a book by the same name. Other than that, I cannot recognize the book that I wrote. My real book is an exchange of letters with an imaginary Darwin to discuss discoveries in modern biology that, I maintain, significantly enrich our understanding of how and why evolution takes place. At the heart of my thesis is the idea that we will not understand evolved organisms until we understand both the internal genomic forces and the external ecological forces that shape the emergence of unique phenotypes from unique genotypes. I describe the multitrack nature of evolution and modern developmental genetics and discuss the naivety of prevailing arguments about genetic determinism in biology, in general, and in human nature and individuality, in particular. And all of this with literary, musical and personal reminiscences, and humour. Charlesworth contracts my ideas to unrecognizable straw-men that I ‘have disposed of natural selection, except as a relatively feeble force’; that ‘molecular drive is a major (if not the major) force in evolution’; that I assert ‘the primacy of biased gene conversion over other evolutionary forces’; that ‘selection is ineffective in preventing the process of spread [by biased gene conversion], even if the variants in question reduce fitness’ and so on. My correspondence with Darwin abundantly discusses the traditional role of selection in solving problems arising from the vagaries of ecology and also its role in solving problems arising from the homogenization (molecular drive) consequences of genomes undergoing ‘turnover’ by six well-characterized mechanisms. By re-examining the one-off nature of selection among unique
phenotypes at each generation, I offer a view of adaptation that circumvents the old problem of tautology, contrary to what Charlesworth says I’m up to. Furthermore, I am as happy with turnover by transposition, unequal crossing over, unbiased gene conversion, slippage and so on3, as I am with biased gene conversion and selection as contributing forces affecting, for example, the regions that regulate the on–off switching of genes. Hence, there is no need for Charlesworth to pit biased gene conversion against selection. All processes are operationally distinct but interact with each other. I repeatedly suggest1,4,5 that the phenomenon of ‘molecular coevolution’ and the origins of many biological novelties arise from the combined forces of natural selection, neutral drift and molecular drive (the last involving all turnover mechanisms and not just biased gene conversion). Importantly, a key section of my thesis is that the newly discovered modular construction of organisms, and the buffering consequences of redundant genetic systems undergoing turnover, facilitate the interaction of natural selection with molecular drive. This is particularly relevant in cases where homogenization is slow and incomplete, allowing members of gene families to functionally differentiate. Charlesworth repeats this as a point scored. Selection is intimately involved all along the line. There is no need to worry, Brian. I don’t know why ‘the rest of the community is unconvinced’, anymore than I suppose Darwin knew why natural selection was not seriously accepted until the advent of mendelian genetics, half a century later, although he lamented ‘great is the power of misrepresentation’. At least, the theory of molecular drive doesn’t need to wait for the extensive evidence of nonmendelian turnover, homogenization and molecular coevolution in modular, redundant systems. They stare us in the face – which makes me wonder why the advocates of novelty-by-selection-only are so seemingly ungracious. There is more to the evolution of biological functions than natural selection and there is more to my book than meets Charlesworth’s eye6. Gabby Dover Dept of Genetics, University of Leicester, Leicester, UK LE1 7RH.
References 1 Dover, G.A. (2000) Dear Mr Darwin: Letters on the Evolution of Life and Human Nature, Weidenfeld & Nicholson and University of California Press 2 Charlesworth, B. (2000) Driving Mr Darwin. Trends Ecol. Evol. 15, 477–478 3 Dover, G.A. (1982) Molecular drive: a cohesive mode of species evolution. Nature 299, 111–117 4 Dover, G.A. and Flavell, R.B. (1984) Molecular coevolution: DNA divergence and the maintenance of function. Cell 38, 623–624 5 Dover, G.A. (2000) How genomic and developmental dynamics affect evolutionary processes. BioEssays 22, 1153–1159 6 Wilkie, T. (2000) Selfish gene is offside. Nat. Genet. 26, 401–402
Corals and phase shifts Comment from Scully & Ostrander
The recent review by Nyström et al.1 nicely summarized our changing view of coral reefs from one of a relatively stable, diverse community to a more dynamic, variable structure that is characterized by phase shifts. The emphasis in the review was on how anthropogenic factors might alter the natural disturbance regime and affect subsequent phase shifts and/or recovery. The challenge, however, is in understanding the natural disturbance regime of the community and identifying the influence, if any, of human activities. Furthermore, we need to document precisely the time scale of phase shifts. The most commonly observed phase shift in reefs is from a state where hermatypic corals predominate to a condition in which fleshy macroalgae occupy a considerable portion of the substrate. The interaction between corals and macroalgae is complex2. Not only are we dealing with taxa possessing completely different life histories, but also with factors that either inhibit or benefit one group but which will not necessarily have the converse effect on the other group. Thus, we have a community in which direct (competition for space) and indirect effects (impact of corallivores or herbivores) are equally important. Nyström et al.1 summarized the phase shift in Caribbean reefs and discussed in some detail the case of Jamaica. The combined effects of anthropogenic factors (overfishing and nutrient enrichment) and hurricane damage were clear, and the time
http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
News & Comment
scale of the transition was measured in years3. Phase shifts, however, can occur over much shorter time scales and there might not be discernible human influences. The western forereef of San Salvador Island (Bahamas) experienced a coral– macroalgae phase shift from 1994 to 19984, with the most pronounced changes occurring in less than six months. There was a mass bleaching episode in 1994, and a major hurricane impact in 1996. The bleaching episode, however, might have been only one contributing factor in the phase shift and the hurricane had little effect on subsequent community composition. There were no identifiable anthropogenic factors that could be linked to this event. Furthermore, shallow patch reefs around San Salvador also experienced a bleaching event, did not undergo a phase shift, and had a much better rate of coral recovery5. This event underscores the point of Nyström et al. that there is a wide range in both the spatial and temporal scales of coral reef disturbance, and that the San Salvador case appears to be at the lower end of these scales. The large variability of coral reef communities over a range of scales means that research efforts to understand their dynamics must study reefs across this range. Programs to address regional issues must be coupled with survey regimes designed to quantify variability within communities, and they both must be planned as long-term efforts. In addition, we will have to examine global, possibly anthropogenic, atmospheric effects, including global warming6, elevated carbon dioxide7 and dust8. Anything less than such a broad, systematic effort will limit our understanding of coral reefs to a list of post-hoc hypotheses and a few welldocumented cases. Erik P. Scully* Biology Dept, Towson University, Towson, MD 21252, USA. *e-mail: [email protected] Gary K. Ostrander Dept of Biology and Division of Comparative Medicine, The Johns Hopkins University, Baltimore, MD 21218, USA. References 1 Nyström, M. et al. (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15, 413–417 2 Miller, M.W. (1998) Coral/seaweed competition and the control of reef community structure
TRENDS in Ecology & Evolution Vol.16 No.3 March 2001
3
4
5
6 7
8
within and between latitudes. Oceanogr. Mar. Biol. Ann. Rev. 36, 65–96 Hughes, T.P. (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265, 1547–1551 Ostrander, G.K. et al. (2000) Rapid transition in the structure of a coral reef community: the effects of coral bleaching and physical disturbance. Proc. Natl. Acad. Sci. U. S. A. 97, 5297–5302 McGrath, T.A. and Smith, G.W. (1998) The effects of the 1995/1996 Western Atlantic coral bleaching event on the patch reefs around San Salvador, Bahamas. Rev. Biol. Trop. 46 (Suppl.), 91–99 Normile, D. (2000) Warmer waters more deadly to coral reefs than pollution. Science 290, 682–683 Kleypas, J.A. et al. (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284, 118–120 Shinn, E.A. et al. (2000) African dust and the demise of Caribbean coral reefs. Geophys. Res. Lett. 27, 3029–3032
Corals and phase shifts Reply from Nyström, Folke & Moberg
We welcome the comments made by Scully and Ostrander, which highlight that phase shifts can occur in coral areas that are not under immediate anthropogenic influence, and that they might be a natural ingredient in the dynamics of modern coral reefs. To understand such changes, we do indeed need to address the influence of natural disturbance regimes on coral reef communities, and learn more about the complex interactions between corals and macroalgae. Unfortunately, there might only be few, if any, pristine coral reefs left on which to study phaseshifts and natural disturbance regimes [Refs 1,2 and see Bryant, D. et al. (1998) Reefs at risk. A map-based indicator of potential threats to the world’s coral reefs: http://www.wri.org/wri/indictrs/reefrisk. htm]. A major point in our review3 was that these shifts seem to have become more frequent and less reversible because of human impacts and that humans might also alter the magnitude, frequency and duration of disturbance regimes. Many of the world’s coral reefs assumed to be pristine show signs of overfishing of highly valued predatory fishes4 and might already have been overfished when intensive scientific investigations began1. In addition, reefs with no discernible human influences might suffer from indirect human influence at scales that reach far beyond the border of the individual reef, such as global
127
warming, increased levels of carbon dioxide5 and dust6. Subtle interactions of a number of factors7 can lead to a loss of ecosystem resilience that is difficult to detect until a reef shifts to another stability domain caused by a disturbance that could previously be absorbed8. Thus, what we experience as a fast transition (within months) from one state to another might be the result of a long-term gradual change over years, decades or even centuries. This raises some key questions for future research. How do we detect gradual loss of resilience and how can we qualitatively and quantitatively measure such loss, and incorporate this knowledge in the management of coral reefs? Our understanding of factors that might signal loss of resilience is, however, still in its infancy. In order to secure the ability of coral reefs to provide humans with ecological goods and services9, we must understand the properties that enable coral reef ecosystems to maintain their resilience in the face of an increasingly humandominated world with altered disturbance regimes3. Magnus Nyström* Carl Folke Fredrik Moberg Dept of Systems Ecology, Stockholm University, S-106 91 Stockholm, Sweden. *[email protected] References 1 Jackson, J.B.C. (1997). Reefs since Columbus. Coral Reefs 16 (Suppl.), 23–32 2 Hatcher, B.G. (1999) Varieties of science for coral reef management. Coral Reefs 18, 305–306 3 Nyström, M. et al. (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15, 413–417 4 McManus, J.W. et al. (2000) Coral reef fishing and coral-algal phase shifts: implications for global reef status. ICES J. Mar. Sci. 57, 572–578 5 Wilkinson, C.R. (2000) Executive summary. In Status of the Coral Reefs of the World: 2000 (Wilkinson C.R., ed), pp. 7–19, Australian Institute of Marine Science 6 Shinn, E.A. et al. (2000) African dust and the demise of Caribbean coral reefs. Geophys. Res. Lett. 27, 3029–3032 7 Ostrander, G.K. et al. (2000) Rapid transition in the structure of a coral reef community: The effects of coral bleaching and physical disturbance. Proc. Natl. Acad. Sci. U. S. A. 97, 5297–5302 8 McCook, L.J. (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357–367 9 Moberg, F. and Folke, C. (1999) Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233
http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
News & Comment
TRENDS in Ecology & Evolution Vol.16 No.3 March 2001
Letters
Dear Mr Darwin: Help! Comment from Dover
I wrote a book called Dear Mr Darwin1. Brian Charlesworth has written a review2 of a book by the same name. Other than that, I cannot recognize the book that I wrote. My real book is an exchange of letters with an imaginary Darwin to discuss discoveries in modern biology that, I maintain, significantly enrich our understanding of how and why evolution takes place. At the heart of my thesis is the idea that we will not understand evolved organisms until we understand both the internal genomic forces and the external ecological forces that shape the emergence of unique phenotypes from unique genotypes. I describe the multitrack nature of evolution and modern developmental genetics and discuss the naivety of prevailing arguments about genetic determinism in biology, in general, and in human nature and individuality, in particular. And all of this with literary, musical and personal reminiscences, and humour. Charlesworth contracts my ideas to unrecognizable straw-men that I ‘have disposed of natural selection, except as a relatively feeble force’; that ‘molecular drive is a major (if not the major) force in evolution’; that I assert ‘the primacy of biased gene conversion over other evolutionary forces’; that ‘selection is ineffective in preventing the process of spread [by biased gene conversion], even if the variants in question reduce fitness’ and so on. My correspondence with Darwin abundantly discusses the traditional role of selection in solving problems arising from the vagaries of ecology and also its role in solving problems arising from the homogenization (molecular drive) consequences of genomes undergoing ‘turnover’ by six well-characterized mechanisms. By re-examining the one-off nature of selection among unique
phenotypes at each generation, I offer a view of adaptation that circumvents the old problem of tautology, contrary to what Charlesworth says I’m up to. Furthermore, I am as happy with turnover by transposition, unequal crossing over, unbiased gene conversion, slippage and so on3, as I am with biased gene conversion and selection as contributing forces affecting, for example, the regions that regulate the on–off switching of genes. Hence, there is no need for Charlesworth to pit biased gene conversion against selection. All processes are operationally distinct but interact with each other. I repeatedly suggest1,4,5 that the phenomenon of ‘molecular coevolution’ and the origins of many biological novelties arise from the combined forces of natural selection, neutral drift and molecular drive (the last involving all turnover mechanisms and not just biased gene conversion). Importantly, a key section of my thesis is that the newly discovered modular construction of organisms, and the buffering consequences of redundant genetic systems undergoing turnover, facilitate the interaction of natural selection with molecular drive. This is particularly relevant in cases where homogenization is slow and incomplete, allowing members of gene families to functionally differentiate. Charlesworth repeats this as a point scored. Selection is intimately involved all along the line. There is no need to worry, Brian. I don’t know why ‘the rest of the community is unconvinced’, anymore than I suppose Darwin knew why natural selection was not seriously accepted until the advent of mendelian genetics, half a century later, although he lamented ‘great is the power of misrepresentation’. At least, the theory of molecular drive doesn’t need to wait for the extensive evidence of nonmendelian turnover, homogenization and molecular coevolution in modular, redundant systems. They stare us in the face – which makes me wonder why the advocates of novelty-by-selection-only are so seemingly ungracious. There is more to the evolution of biological functions than natural selection and there is more to my book than meets Charlesworth’s eye6. Gabby Dover Dept of Genetics, University of Leicester, Leicester, UK LE1 7RH.
References 1 Dover, G.A. (2000) Dear Mr Darwin: Letters on the Evolution of Life and Human Nature, Weidenfeld & Nicholson and University of California Press 2 Charlesworth, B. (2000) Driving Mr Darwin. Trends Ecol. Evol. 15, 477–478 3 Dover, G.A. (1982) Molecular drive: a cohesive mode of species evolution. Nature 299, 111–117 4 Dover, G.A. and Flavell, R.B. (1984) Molecular coevolution: DNA divergence and the maintenance of function. Cell 38, 623–624 5 Dover, G.A. (2000) How genomic and developmental dynamics affect evolutionary processes. BioEssays 22, 1153–1159 6 Wilkie, T. (2000) Selfish gene is offside. Nat. Genet. 26, 401–402
Corals and phase shifts Comment from Scully & Ostrander
The recent review by Nyström et al.1 nicely summarized our changing view of coral reefs from one of a relatively stable, diverse community to a more dynamic, variable structure that is characterized by phase shifts. The emphasis in the review was on how anthropogenic factors might alter the natural disturbance regime and affect subsequent phase shifts and/or recovery. The challenge, however, is in understanding the natural disturbance regime of the community and identifying the influence, if any, of human activities. Furthermore, we need to document precisely the time scale of phase shifts. The most commonly observed phase shift in reefs is from a state where hermatypic corals predominate to a condition in which fleshy macroalgae occupy a considerable portion of the substrate. The interaction between corals and macroalgae is complex2. Not only are we dealing with taxa possessing completely different life histories, but also with factors that either inhibit or benefit one group but which will not necessarily have the converse effect on the other group. Thus, we have a community in which direct (competition for space) and indirect effects (impact of corallivores or herbivores) are equally important. Nyström et al.1 summarized the phase shift in Caribbean reefs and discussed in some detail the case of Jamaica. The combined effects of anthropogenic factors (overfishing and nutrient enrichment) and hurricane damage were clear, and the time
http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
News & Comment
scale of the transition was measured in years3. Phase shifts, however, can occur over much shorter time scales and there might not be discernible human influences. The western forereef of San Salvador Island (Bahamas) experienced a coral– macroalgae phase shift from 1994 to 19984, with the most pronounced changes occurring in less than six months. There was a mass bleaching episode in 1994, and a major hurricane impact in 1996. The bleaching episode, however, might have been only one contributing factor in the phase shift and the hurricane had little effect on subsequent community composition. There were no identifiable anthropogenic factors that could be linked to this event. Furthermore, shallow patch reefs around San Salvador also experienced a bleaching event, did not undergo a phase shift, and had a much better rate of coral recovery5. This event underscores the point of Nyström et al. that there is a wide range in both the spatial and temporal scales of coral reef disturbance, and that the San Salvador case appears to be at the lower end of these scales. The large variability of coral reef communities over a range of scales means that research efforts to understand their dynamics must study reefs across this range. Programs to address regional issues must be coupled with survey regimes designed to quantify variability within communities, and they both must be planned as long-term efforts. In addition, we will have to examine global, possibly anthropogenic, atmospheric effects, including global warming6, elevated carbon dioxide7 and dust8. Anything less than such a broad, systematic effort will limit our understanding of coral reefs to a list of post-hoc hypotheses and a few welldocumented cases. Erik P. Scully* Biology Dept, Towson University, Towson, MD 21252, USA. *e-mail: [email protected] Gary K. Ostrander Dept of Biology and Division of Comparative Medicine, The Johns Hopkins University, Baltimore, MD 21218, USA. References 1 Nyström, M. et al. (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15, 413–417 2 Miller, M.W. (1998) Coral/seaweed competition and the control of reef community structure
TRENDS in Ecology & Evolution Vol.16 No.3 March 2001
3
4
5
6 7
8
within and between latitudes. Oceanogr. Mar. Biol. Ann. Rev. 36, 65–96 Hughes, T.P. (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265, 1547–1551 Ostrander, G.K. et al. (2000) Rapid transition in the structure of a coral reef community: the effects of coral bleaching and physical disturbance. Proc. Natl. Acad. Sci. U. S. A. 97, 5297–5302 McGrath, T.A. and Smith, G.W. (1998) The effects of the 1995/1996 Western Atlantic coral bleaching event on the patch reefs around San Salvador, Bahamas. Rev. Biol. Trop. 46 (Suppl.), 91–99 Normile, D. (2000) Warmer waters more deadly to coral reefs than pollution. Science 290, 682–683 Kleypas, J.A. et al. (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284, 118–120 Shinn, E.A. et al. (2000) African dust and the demise of Caribbean coral reefs. Geophys. Res. Lett. 27, 3029–3032
Corals and phase shifts Reply from Nyström, Folke & Moberg
We welcome the comments made by Scully and Ostrander, which highlight that phase shifts can occur in coral areas that are not under immediate anthropogenic influence, and that they might be a natural ingredient in the dynamics of modern coral reefs. To understand such changes, we do indeed need to address the influence of natural disturbance regimes on coral reef communities, and learn more about the complex interactions between corals and macroalgae. Unfortunately, there might only be few, if any, pristine coral reefs left on which to study phaseshifts and natural disturbance regimes [Refs 1,2 and see Bryant, D. et al. (1998) Reefs at risk. A map-based indicator of potential threats to the world’s coral reefs: http://www.wri.org/wri/indictrs/reefrisk. htm]. A major point in our review3 was that these shifts seem to have become more frequent and less reversible because of human impacts and that humans might also alter the magnitude, frequency and duration of disturbance regimes. Many of the world’s coral reefs assumed to be pristine show signs of overfishing of highly valued predatory fishes4 and might already have been overfished when intensive scientific investigations began1. In addition, reefs with no discernible human influences might suffer from indirect human influence at scales that reach far beyond the border of the individual reef, such as global
127
warming, increased levels of carbon dioxide5 and dust6. Subtle interactions of a number of factors7 can lead to a loss of ecosystem resilience that is difficult to detect until a reef shifts to another stability domain caused by a disturbance that could previously be absorbed8. Thus, what we experience as a fast transition (within months) from one state to another might be the result of a long-term gradual change over years, decades or even centuries. This raises some key questions for future research. How do we detect gradual loss of resilience and how can we qualitatively and quantitatively measure such loss, and incorporate this knowledge in the management of coral reefs? Our understanding of factors that might signal loss of resilience is, however, still in its infancy. In order to secure the ability of coral reefs to provide humans with ecological goods and services9, we must understand the properties that enable coral reef ecosystems to maintain their resilience in the face of an increasingly humandominated world with altered disturbance regimes3. Magnus Nyström* Carl Folke Fredrik Moberg Dept of Systems Ecology, Stockholm University, S-106 91 Stockholm, Sweden. *[email protected] References 1 Jackson, J.B.C. (1997). Reefs since Columbus. Coral Reefs 16 (Suppl.), 23–32 2 Hatcher, B.G. (1999) Varieties of science for coral reef management. Coral Reefs 18, 305–306 3 Nyström, M. et al. (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15, 413–417 4 McManus, J.W. et al. (2000) Coral reef fishing and coral-algal phase shifts: implications for global reef status. ICES J. Mar. Sci. 57, 572–578 5 Wilkinson, C.R. (2000) Executive summary. In Status of the Coral Reefs of the World: 2000 (Wilkinson C.R., ed), pp. 7–19, Australian Institute of Marine Science 6 Shinn, E.A. et al. (2000) African dust and the demise of Caribbean coral reefs. Geophys. Res. Lett. 27, 3029–3032 7 Ostrander, G.K. et al. (2000) Rapid transition in the structure of a coral reef community: The effects of coral bleaching and physical disturbance. Proc. Natl. Acad. Sci. U. S. A. 97, 5297–5302 8 McCook, L.J. (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357–367 9 Moberg, F. and Folke, C. (1999) Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233
http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.