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The ‘handicap principle’ works without Fisher
TREE vol. 2, no. 1, January )JM 02 0
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PH Fig. 2 Cyanobacterial mat from Guerrero Negro, Baja, California, showing chemical profiles and oxygenic photosynthesis. A band of Beggiatoa occurs at the 02/H2S interface. Reproduced, with permission, from Ref. 9.
reveal that the Beggiatoa layer is positioned exactly where the oxygen and sulphide levels come together at close to zero (Fig. 2).
Why, in this case, does Beggiatoa occupy the usual position of phototrophic bacteria? The answer was sought in the availability of light, employing a very recently developed technique of measuring spectral light gradients within the mat (using a fibre optic microprobe as described by Jorgensen and Des Marais”). It turned out that at the oxic-anoxic interface, light of a wavelength suitable for phototrophic bacteria was no longer detectable. Comparison with a mat in another pond which did contain a layer of phototrophic sulphur bacteria revealed that this layer did receive at least l-2% of the incident light of the appropriate wavelength. This difference in light intensity is at least partly explained by the height of the water column (up to 1 m and less than 30 cm, respectively) strongly absorbing near infrared light (750-900 nm). A very interesting implication of these results, though not discussed by the authors, is the fact that if there is enough light of appropriate wavelengths then phototrophic sulphur bacteria do appear to outcompete colourless non-phototrophic sulphur bacteria for sulphide, their common growth-limiting substrate. Without these new and sophisticated techniques for studying microbial ecosystems in the field, such a result could not have been obtained; so far it has proved impossible to study
Principle’ Works The‘Handicap Without Fisher Andrew Pomiankowski The evolution of extravagant male ornamentation and display, like the plumage of male peacocks and birds of paradise, is a very controversial area of sexual selection’. A crucial issue is the role of female choice: is it purely aesthetic or is it sensitive to male genetic quality? The ‘aesthetic’ view, that extravagant has male ornamentation evolved simply because females prefer to mate with ornamented males, was first proposed by Darwin2. It was elaborated by Fishe?, who showed that female choice has a selfescalating property: if some females show preference, then males with
Andrew Pomiankowski is at the Department of Biological Sciences, Sussex University, Falmer, Brighton, Sussex BNI 9QG, UK. 2
1987
the preferred trait get more mates. Choosy females (i.e. those with more intense preferences) also do better because their sons are more likely to have the trait and therefore get more mates too. Once started, an increase in the intensity of female preference could lead to a ‘runaway’ exaggeration of the preferred male character, even to a maladaptive extreme. However, the neatness of the Fisher process need not mean that it is the main or only way in which extravagant traits and preferences evolve. In 1975 an alternative process- the ‘handicap principle’ - was proposed by Zahav?; he claimed that female choice of male ornaments that handicapped male survival made adaptive sense because only those males with high viability in other 0 1987. Elsevwr
Beggiatoa in the laboratory. These techniques allow the measurement of light and chemical gradients and microbial activities within hitherto inaccessible microenvironments, and offer exciting prospects for future studies of microbial ecosystems.
References 1 Javor, B. and Castenholz, R.W. (1981) Geomicrobiol. J. 3.237-273 2 Krumbein, W.E., Cohen, Y. and Shilo, Y. (1977) Limnol. Oceanogr. 22,635-656 3 Jorgensen, B.B., Revsbech, N.P. and Cohen, Y. (1983) Limnol. Oceanogr. 28, 1075-1093 4 Krumbein, W.E. and Cohen, Y. (1974)
Geol. Rundschau 63,1035-l 065 5 Gerdes, G. and Krumbien, W.E. (1984) in Microbial Mats: Stromatolites (Cohen, Y., Castenholz, R.W. and Halvorson, H.O., eds), pp. 59-83, Alan R. Liss 6 Castenholz, R.W. (1984) in Microbial Mats: Stromatolites (Cohen, Y., Castenholz, R.W. and Halvorson, H.O., eds), pp. 101-l 19, Alan R. Liss 7 Stal, L.J., van Gemerden, H. and Krumbein, W.E. (1985) FEMS Microbial.
Ecol. 31,111-125 8 Revsbech, N.P., Jergensen, B.B., Blackburn,T.H. and Cohen, Y. (1983) Limnol. Oceanogr. 28,1062-l 074 9 Jorgensen, B.B. and Des Marais, D.J. (1986) FEMS Microbial. Ecol. 38, 178-l 86 10 Jergensen, B.B. and Des Marais, D.J. Limnol. Oceanogr. (in press)
respects could survive with the burden of the handicap. So, a female who preferred ornamented males would tend to have offspring with higher than average viability. However, most evolutionary biologists rejected the handicap principle as a significant evolutionary forcesto. This was for two main reasons. First, population genetics theory predicts that populations close to or at equilibrium will have zero or very low levels of additive variance in fitness7. This, however, is a weak and overstated objection; there are a number of possible ways of maintaining significant levels of fitness variation: recurrent mutation (both deleterious and beneficial), migration and spatially varying selection pressures, and temporally varying selection pressures - particularly those caused by host-parasite coadaptive cycles”. What is more, just because there is no variance in fitness now, it does not follow that there has been none in the past: else, how would occurred? Science
adaptive
Publishers B V, Amsterdam
evolution
016%5347’87;%0
have
200
TREE vol. 2, no. 7, January
1987
The second objection is more important. Models of the handicap principle have shown that it does not substantially alter the conditions for the spread of female preference beyond those predicted by Fisher’s process, and when Fisher’s process does not occur (e.g. with monogamous mating) the handicap principle has no significant effects”‘. This second objection is addressed in an important new paper by Andersson’2. First we need to clarify Zahavi’s original idea. It has been divided into three, not mutually exclusive, types’. A Zahavi handicap assumes that there are strong interactions between genes for the ornament and genes for health, vigour and survival (i.e. viability). Ornamented males with low viability suffer greater mortality than would be expected were there no interaction. This leads to a positive correlation between genes for ornament and viability in adults. A revealing handicap is an ornament that accurately displays male viability; this was proposed by Hamilton and Zuk” for the specific case in which the ornament reveals the degree of past or present parasitism, but it could apply to other cases. A condition-dependent handicap is an ornament that is only developed in males with high viability because its development depends on the general condition of its possessor. Andersson presents the first detailed analysis of condition-dependent handicaps, using analytical and simulation studies of a three-locus model of sexual selection (preference, sex-trait, viability loci). To avoid conflation with the effects of Fisher’s process, he uses a monogamous breeding system in which all males mate and have the same number of offspring, so no individual male has a reproductive advantage. In the first generation, the approximate condition for the spread of female preference is that the increase in survival attributable to heritable variation in viability (e) must be greater than half the reduction in survival caused by the ornament (p), i.e. E > p/2. This is a lax condition which is likely to be easily met in nature. It is especially lax when compared to the condition required for the spread of female preference for a rigid, conditionindependent ornament (i.e. Zahavi handicap) -that t must be very much greater than p (Ref. 8). A similar pattern emerges from simulations of subsequent generations. This is an important result. It shows that female choice for markers of male genetic quality can by
itself (without the help of the Fisher process) easily lead to exaggeration of male ornamentation and female preference when the expression of the marker is condition-dependent. The opposite conclusion was drawn from earlier genetic models of condition-independent ornaments with both monogamous and polygamous breeding systems5-‘o. The next stage for theoreticians is to establish what type of handicap, whether Zahavi, revealing or condition-dependent, is most likely to cause the evolution of extravagant ornamentation. Andersson has begun to unravel this question; he has shown in monogamous mating systems that female preference for condition-dependent male ornaments is more likely to evolve than preference for Zahavi handicaps, that is, for ornaments produced irrespective of male viability.
References 1 Majerus, M.E.N. (1986) Trendsfcol. E vol. 1, 1-7 2 Darwin, C. (1871) TheDescentofMan, John Murray 3 Fisher, R.A. (1930) The Genetical Theory of Natural Selection, Clarendon Press 4 Zahavi, A. (1975) J. Theor. Dol. 53, 205-214 5 Davis, J. and O’Donald, P. (1976) J. Theor. Biol. 57,345-354 6 Maynard Smith, J. (1976) J. Theor. Biol. 57,239-242 7 Maynard 115,1-8
Smith, J. (1985) J. Theor. Biol.
8 Bell, G. (1978) Evolution 9 Andersson, 17,375-393 10 Kirkpatrick, 222-240
32,872-885
M. (1982) Biol. J. Linn. Sot. M. (1986)Am.
Nat. 127,
11 Hamiton, W.D. and Zuk, M. (1982) Science 218,384-387 12 Andersson,
M. Evolution40
(in press)
Bioenergetics: Linking Ecology, Biochemistry andEvolutionary Theory Cohn R. Townsend Organisms can be viewed as resource transformers that partition a finite input of resource between the metabolic compartments of storage, growth, repair, reproduction, defence and foraging (to obtain further resources). The way in which resources are allocated is critical to the fitness of the individual. More resource allocated to storage may increase the organism’s ability to survive periods without food; more to growth may give a bigger body size which may, in turn, reduce the risk of predation and ultimately lead to greater reproductive returns; more to reproduction is likely to give a greater rate of reproduction in the shorter term. The optimum pattern of allocation is the one that, in the prevailing environmental circumstances, most effectively transforms resource input to reproductive output and thus transmits more genes to future generations. Fitness is properly measured as the proportionate contribution of genes to future generations and clearly the ideal would be to calibrate each energy transaction in terms of its effects on reproductive success.
Colin Townsend is at the School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK. 69
5347 87’$0 200
However, it is not generally possible to determine the influence of minute by minute events on the eventual demographic outcome, so it is necessary to define more immediate characteristics that should be strongly correlated with the rate and success of gene transmission. Obvious candidates are the efficiency and/or rate at which energy is made available for the production of new protoplasm by a particular acquisition or allocation strategy. Ecologists have concentrated their attention on strategies for acquirin resources (optimal foraging theory’, B, optimal leaf shape3) and the macroscopic aspects of the optimal allocation of resources to the various possible uses (life-history theory4). But they have largely ignored the metabolic details of resource processing and the biochemical aspects of allocation. Recently, Watt5 has sought to bridge this gap by asking ‘What general measures of metabolic performance can be shown to function as bioenergetic fitness indexes?’ Watt begins by drawing a contrast between metabolic processing power (rate of production of metabolic currency available for allocation) and processing efficiency (currency produced per unit input). Metabolic currencies are limited in number - ATP 3
200
400
600 PM
0
200 I
400
mm-’ 800 02 800
600
2o-a\,\ , 0
100
300
200
400
1000
500
P’M H25 70
75
80
65
90
95
100
PH Fig. 2 Cyanobacterial mat from Guerrero Negro, Baja, California, showing chemical profiles and oxygenic photosynthesis. A band of Beggiatoa occurs at the 02/H2S interface. Reproduced, with permission, from Ref. 9.
reveal that the Beggiatoa layer is positioned exactly where the oxygen and sulphide levels come together at close to zero (Fig. 2).
Why, in this case, does Beggiatoa occupy the usual position of phototrophic bacteria? The answer was sought in the availability of light, employing a very recently developed technique of measuring spectral light gradients within the mat (using a fibre optic microprobe as described by Jorgensen and Des Marais”). It turned out that at the oxic-anoxic interface, light of a wavelength suitable for phototrophic bacteria was no longer detectable. Comparison with a mat in another pond which did contain a layer of phototrophic sulphur bacteria revealed that this layer did receive at least l-2% of the incident light of the appropriate wavelength. This difference in light intensity is at least partly explained by the height of the water column (up to 1 m and less than 30 cm, respectively) strongly absorbing near infrared light (750-900 nm). A very interesting implication of these results, though not discussed by the authors, is the fact that if there is enough light of appropriate wavelengths then phototrophic sulphur bacteria do appear to outcompete colourless non-phototrophic sulphur bacteria for sulphide, their common growth-limiting substrate. Without these new and sophisticated techniques for studying microbial ecosystems in the field, such a result could not have been obtained; so far it has proved impossible to study
Principle’ Works The‘Handicap Without Fisher Andrew Pomiankowski The evolution of extravagant male ornamentation and display, like the plumage of male peacocks and birds of paradise, is a very controversial area of sexual selection’. A crucial issue is the role of female choice: is it purely aesthetic or is it sensitive to male genetic quality? The ‘aesthetic’ view, that extravagant has male ornamentation evolved simply because females prefer to mate with ornamented males, was first proposed by Darwin2. It was elaborated by Fishe?, who showed that female choice has a selfescalating property: if some females show preference, then males with
Andrew Pomiankowski is at the Department of Biological Sciences, Sussex University, Falmer, Brighton, Sussex BNI 9QG, UK. 2
1987
the preferred trait get more mates. Choosy females (i.e. those with more intense preferences) also do better because their sons are more likely to have the trait and therefore get more mates too. Once started, an increase in the intensity of female preference could lead to a ‘runaway’ exaggeration of the preferred male character, even to a maladaptive extreme. However, the neatness of the Fisher process need not mean that it is the main or only way in which extravagant traits and preferences evolve. In 1975 an alternative process- the ‘handicap principle’ - was proposed by Zahav?; he claimed that female choice of male ornaments that handicapped male survival made adaptive sense because only those males with high viability in other 0 1987. Elsevwr
Beggiatoa in the laboratory. These techniques allow the measurement of light and chemical gradients and microbial activities within hitherto inaccessible microenvironments, and offer exciting prospects for future studies of microbial ecosystems.
References 1 Javor, B. and Castenholz, R.W. (1981) Geomicrobiol. J. 3.237-273 2 Krumbein, W.E., Cohen, Y. and Shilo, Y. (1977) Limnol. Oceanogr. 22,635-656 3 Jorgensen, B.B., Revsbech, N.P. and Cohen, Y. (1983) Limnol. Oceanogr. 28, 1075-1093 4 Krumbein, W.E. and Cohen, Y. (1974)
Geol. Rundschau 63,1035-l 065 5 Gerdes, G. and Krumbien, W.E. (1984) in Microbial Mats: Stromatolites (Cohen, Y., Castenholz, R.W. and Halvorson, H.O., eds), pp. 59-83, Alan R. Liss 6 Castenholz, R.W. (1984) in Microbial Mats: Stromatolites (Cohen, Y., Castenholz, R.W. and Halvorson, H.O., eds), pp. 101-l 19, Alan R. Liss 7 Stal, L.J., van Gemerden, H. and Krumbein, W.E. (1985) FEMS Microbial.
Ecol. 31,111-125 8 Revsbech, N.P., Jergensen, B.B., Blackburn,T.H. and Cohen, Y. (1983) Limnol. Oceanogr. 28,1062-l 074 9 Jorgensen, B.B. and Des Marais, D.J. (1986) FEMS Microbial. Ecol. 38, 178-l 86 10 Jergensen, B.B. and Des Marais, D.J. Limnol. Oceanogr. (in press)
respects could survive with the burden of the handicap. So, a female who preferred ornamented males would tend to have offspring with higher than average viability. However, most evolutionary biologists rejected the handicap principle as a significant evolutionary forcesto. This was for two main reasons. First, population genetics theory predicts that populations close to or at equilibrium will have zero or very low levels of additive variance in fitness7. This, however, is a weak and overstated objection; there are a number of possible ways of maintaining significant levels of fitness variation: recurrent mutation (both deleterious and beneficial), migration and spatially varying selection pressures, and temporally varying selection pressures - particularly those caused by host-parasite coadaptive cycles”. What is more, just because there is no variance in fitness now, it does not follow that there has been none in the past: else, how would occurred? Science
adaptive
Publishers B V, Amsterdam
evolution
016%5347’87;%0
have
200
TREE vol. 2, no. 7, January
1987
The second objection is more important. Models of the handicap principle have shown that it does not substantially alter the conditions for the spread of female preference beyond those predicted by Fisher’s process, and when Fisher’s process does not occur (e.g. with monogamous mating) the handicap principle has no significant effects”‘. This second objection is addressed in an important new paper by Andersson’2. First we need to clarify Zahavi’s original idea. It has been divided into three, not mutually exclusive, types’. A Zahavi handicap assumes that there are strong interactions between genes for the ornament and genes for health, vigour and survival (i.e. viability). Ornamented males with low viability suffer greater mortality than would be expected were there no interaction. This leads to a positive correlation between genes for ornament and viability in adults. A revealing handicap is an ornament that accurately displays male viability; this was proposed by Hamilton and Zuk” for the specific case in which the ornament reveals the degree of past or present parasitism, but it could apply to other cases. A condition-dependent handicap is an ornament that is only developed in males with high viability because its development depends on the general condition of its possessor. Andersson presents the first detailed analysis of condition-dependent handicaps, using analytical and simulation studies of a three-locus model of sexual selection (preference, sex-trait, viability loci). To avoid conflation with the effects of Fisher’s process, he uses a monogamous breeding system in which all males mate and have the same number of offspring, so no individual male has a reproductive advantage. In the first generation, the approximate condition for the spread of female preference is that the increase in survival attributable to heritable variation in viability (e) must be greater than half the reduction in survival caused by the ornament (p), i.e. E > p/2. This is a lax condition which is likely to be easily met in nature. It is especially lax when compared to the condition required for the spread of female preference for a rigid, conditionindependent ornament (i.e. Zahavi handicap) -that t must be very much greater than p (Ref. 8). A similar pattern emerges from simulations of subsequent generations. This is an important result. It shows that female choice for markers of male genetic quality can by
itself (without the help of the Fisher process) easily lead to exaggeration of male ornamentation and female preference when the expression of the marker is condition-dependent. The opposite conclusion was drawn from earlier genetic models of condition-independent ornaments with both monogamous and polygamous breeding systems5-‘o. The next stage for theoreticians is to establish what type of handicap, whether Zahavi, revealing or condition-dependent, is most likely to cause the evolution of extravagant ornamentation. Andersson has begun to unravel this question; he has shown in monogamous mating systems that female preference for condition-dependent male ornaments is more likely to evolve than preference for Zahavi handicaps, that is, for ornaments produced irrespective of male viability.
References 1 Majerus, M.E.N. (1986) Trendsfcol. E vol. 1, 1-7 2 Darwin, C. (1871) TheDescentofMan, John Murray 3 Fisher, R.A. (1930) The Genetical Theory of Natural Selection, Clarendon Press 4 Zahavi, A. (1975) J. Theor. Dol. 53, 205-214 5 Davis, J. and O’Donald, P. (1976) J. Theor. Biol. 57,345-354 6 Maynard Smith, J. (1976) J. Theor. Biol. 57,239-242 7 Maynard 115,1-8
Smith, J. (1985) J. Theor. Biol.
8 Bell, G. (1978) Evolution 9 Andersson, 17,375-393 10 Kirkpatrick, 222-240
32,872-885
M. (1982) Biol. J. Linn. Sot. M. (1986)Am.
Nat. 127,
11 Hamiton, W.D. and Zuk, M. (1982) Science 218,384-387 12 Andersson,
M. Evolution40
(in press)
Bioenergetics: Linking Ecology, Biochemistry andEvolutionary Theory Cohn R. Townsend Organisms can be viewed as resource transformers that partition a finite input of resource between the metabolic compartments of storage, growth, repair, reproduction, defence and foraging (to obtain further resources). The way in which resources are allocated is critical to the fitness of the individual. More resource allocated to storage may increase the organism’s ability to survive periods without food; more to growth may give a bigger body size which may, in turn, reduce the risk of predation and ultimately lead to greater reproductive returns; more to reproduction is likely to give a greater rate of reproduction in the shorter term. The optimum pattern of allocation is the one that, in the prevailing environmental circumstances, most effectively transforms resource input to reproductive output and thus transmits more genes to future generations. Fitness is properly measured as the proportionate contribution of genes to future generations and clearly the ideal would be to calibrate each energy transaction in terms of its effects on reproductive success.
Colin Townsend is at the School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK. 69
5347 87’$0 200
However, it is not generally possible to determine the influence of minute by minute events on the eventual demographic outcome, so it is necessary to define more immediate characteristics that should be strongly correlated with the rate and success of gene transmission. Obvious candidates are the efficiency and/or rate at which energy is made available for the production of new protoplasm by a particular acquisition or allocation strategy. Ecologists have concentrated their attention on strategies for acquirin resources (optimal foraging theory’, B, optimal leaf shape3) and the macroscopic aspects of the optimal allocation of resources to the various possible uses (life-history theory4). But they have largely ignored the metabolic details of resource processing and the biochemical aspects of allocation. Recently, Watt5 has sought to bridge this gap by asking ‘What general measures of metabolic performance can be shown to function as bioenergetic fitness indexes?’ Watt begins by drawing a contrast between metabolic processing power (rate of production of metabolic currency available for allocation) and processing efficiency (currency produced per unit input). Metabolic currencies are limited in number - ATP 3