- Email: [email protected]
Lineage selection and the capacity to evolve
r
Medical Hypotheses
I
I
Medical Hypotirar (1991) 35. 155-156 e Lqym GroupUK Lad 1991
Lineage Selection and the Capacity to Evolve F. ABOITIZ Neuroscience Program, Brain Research Institute, California 90024, USA
73-346
CHS, University of California,
Los Angeles.
Abstract - The capacity of genetic recombination is an unusual adaptive trait since it is based on the capacity to produce evolutionary change rather than on the capacity to produce better performing individuals. The evolution of this character has been considered to be a case of group or species selection. Alternatively, I introduce a new concept, lineage selection, to account for the evolution of this trait.
Adaptive evolution usually refers to evolutionary changes occurring as a response to specific circumstances. The Darwinian concept of adaptation through natural selection implies that individuals bearing certain heritable characters may perform better than others in certain behaviors that are critical for survival. This may lead to the differential survival of these individuals and their offspring (1). Other kind of selection may also occur, which is not related with specific performances but solely with the reproductive ability of the individuals bearing the characters. This kind of selection is denominated sexual selection (2). It has been argued that natural selection may act not only at the level of the individual but also at the level of the group, or the population, or the species (3-7). This has been proposed to occur when entire groups or species become extinct and are replaced by related ones (3, 8). However, it is possible that individual properties may be causing group or species extinction. For example, in the evolution of dispersal patterns the ability to disperse may depend on individual characters and this may lead to the differential extinction of whole populations (8). A simpler case is Date received 20 February 1991 Datsz accepted 23 April 1991 \lH
JJ
the competition for resources between related species. Here, competition occurs between individuals of the different species and this produces species extinction. In these instances, group or species extinction appears to be a consequence of individual selection between members of different groups or species. For this reason, Sober (9) has pointed out the existence of group (or population, or species) properties defining the group (species) as an interacting unit. Only if these properties occur, groups (or species) may be selected according to specific environmental conditions. A typical example of such group properties is behavioral cooperation among members of a group. A similar concept has been proposed by Hull (lo), who distinguishes between replicators and interactors. Replicators are genes in the same sense as Dawkins (ll), but selection occurs based on the properties of interactors (which are at least partly determined by genes). In different circumstances, interactors may be individuals, groups or species, depending on the interacting unit in each case. An instance of adaptation in which group and species selection have been invoked as better expla-
155
156 nations than individual selection is the evolution of genetic systems of recombination and mutation. Sexual reproduction (7, 12, 13) and the existence of certain genetic and chromosomic arrangements (such as jumping genes and multigene families (14)) may facilitate the occurrence of functional mutations, thus easing the evolutionary process (7, 14). These traits are different from the classical adaptive characters, which relate to the capacity to perform specific interactions. The increased capacity of genetic recombination relates rather to the capacity to change (or to evolve) and is more strongly selectetd for in conditions of continued environmental change (7, 14). It is argued that it may make no difference for the individual whether it has or not these genetic traits. However, a group of species bearing them is at an advantage over groups or species lacking the trait, since there are more opportunities to produce advantageous variants (7, 14). This approach fails to explain how groups (or species) acquired the trait in the first place. The usual answer is that it has been acquired by chance. Furthermore, it has some difficulties to meet Sober’s criteria for group properties (9). It is difficult to see if these traits are any more group or species properties than, say, genes for a long neck in the case of the giraffe. I suggest that the explanation of the capacity for genetic recombination does not lie in group or species selection. Instead, I will argue that this trait confers advantage to genetic lineages. Suppose that an individual carries a jumping gene that has produced a lucky recombination event that in turn has conferred a better performance to the individual. This subject will be eventually more successful at reproducing. There is no doubt that in this case the selected properties are expressed at the individual level. It makes no real difference whether the mutation was caused by a jumping gene or some other agent. However, if successful mutations tend to occur again and again in the lineage of this individual, then its lineage will be favoured in a variety of circumstances. In every mutational instance, individual properties produce survival, but it is the capacity to produce useful mutations that becomes selected in the long run. This capacity is a property of the lineage and is caused by the presence of jumping genes in this case. In Hull’s terms (10) the selected replicator would be the jumping gene while the interactor would be the lineage of individuals. I propose to call this process lineage selection. An alternative possibility is to consider the jumping gene as both a relicator and an interactor, whose performance in producing useful mutations is the se-
MEDICAL llYF’OTHE8E.S
lected property. However, in each instance, selection occurs based on the properties of individuals and for each of these cases the individual may be considered as the interactor. Lineage selection is a consequence of the iteration of individual selection, however, selecting different properties at each time. In other words, without making a difference in individual performance, jumping genes could not be selected for. Lineage selection may be confused with group or species selection because these concepts usually imply reproductive interactions between individuals (2). However, from what I have argued, if a single individual carries the character it may still spread to the whole population or species because of its adaptive value. Therefore, group selection is clearly not necessary to spread the character. Furthermore, I have proposed that there is no group property that is necessarily produced by the possession of recombinatory characters. Instead, this appears as a property of the lineage. Finally, lineage selection may permit a much faster evolutionary rate than group of species selection, thus explaining the relatively rapid origin of some complex multigene systems. This has been claimed to be difficult to account for within the framework of group or species selection (14). References 1. Aboitiz F. Behavior, archetypes and the irreversibility of evolution. Medical Hypotheses 30: 87. 1989. 2. Eldredge N. Macroevolutionary Dynamics. McGraw Hill, New York, 1989. 3. Wynne-Edwards VC. Animal Dispersion in Relation to Social Behavior. Oliver and Boyd, Edinburgh, 1962. 4. Wvnne-Edwards VC. Evolution Throueh G~OUD Selection. ” a Blackwell Eds., London, 1986. 5. Wilson DS. A theory of group selection. Proceedings of the National Academy of Sciences (USA) 72: 143, 1975. 6. Gould SJ, Eldredge N. Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3: 115, 1977. 7. Stanley SM. Macroevolution. Pattern and Proces. Freeman and Company, San Francisco, 1979. 8. Van Valen L. Group selection and the evolution of dispersal. Evolution 25: 591, 1971. 9. Sober E. The Nature of Selection. Evolutionary Theory in Philosophical Focus. MIT Press, Cambridge, 1984. 10. Hull D. Interactors versus vehicles. pl9 ht The Role of Behavior in Evolution (HC Plotkin. ed.)., MIT Press. Cambridee.Y . 1988. 11. Dawkins R. The Selfish Gene. Oxford Press, Oxford, 1976. 12. Maynard Smith I. The Evolution of Sex. Cambridge Press, Cambridge, 1978. 13. Margulis L. Sagan D. Origins of Sex. Yale Press, New Haven, 1986. 14. Wills C. The Wisdom of the Genes. Basic Books, New York, 1989.
Medical Hypotheses
I
I
Medical Hypotirar (1991) 35. 155-156 e Lqym GroupUK Lad 1991
Lineage Selection and the Capacity to Evolve F. ABOITIZ Neuroscience Program, Brain Research Institute, California 90024, USA
73-346
CHS, University of California,
Los Angeles.
Abstract - The capacity of genetic recombination is an unusual adaptive trait since it is based on the capacity to produce evolutionary change rather than on the capacity to produce better performing individuals. The evolution of this character has been considered to be a case of group or species selection. Alternatively, I introduce a new concept, lineage selection, to account for the evolution of this trait.
Adaptive evolution usually refers to evolutionary changes occurring as a response to specific circumstances. The Darwinian concept of adaptation through natural selection implies that individuals bearing certain heritable characters may perform better than others in certain behaviors that are critical for survival. This may lead to the differential survival of these individuals and their offspring (1). Other kind of selection may also occur, which is not related with specific performances but solely with the reproductive ability of the individuals bearing the characters. This kind of selection is denominated sexual selection (2). It has been argued that natural selection may act not only at the level of the individual but also at the level of the group, or the population, or the species (3-7). This has been proposed to occur when entire groups or species become extinct and are replaced by related ones (3, 8). However, it is possible that individual properties may be causing group or species extinction. For example, in the evolution of dispersal patterns the ability to disperse may depend on individual characters and this may lead to the differential extinction of whole populations (8). A simpler case is Date received 20 February 1991 Datsz accepted 23 April 1991 \lH
JJ
the competition for resources between related species. Here, competition occurs between individuals of the different species and this produces species extinction. In these instances, group or species extinction appears to be a consequence of individual selection between members of different groups or species. For this reason, Sober (9) has pointed out the existence of group (or population, or species) properties defining the group (species) as an interacting unit. Only if these properties occur, groups (or species) may be selected according to specific environmental conditions. A typical example of such group properties is behavioral cooperation among members of a group. A similar concept has been proposed by Hull (lo), who distinguishes between replicators and interactors. Replicators are genes in the same sense as Dawkins (ll), but selection occurs based on the properties of interactors (which are at least partly determined by genes). In different circumstances, interactors may be individuals, groups or species, depending on the interacting unit in each case. An instance of adaptation in which group and species selection have been invoked as better expla-
155
156 nations than individual selection is the evolution of genetic systems of recombination and mutation. Sexual reproduction (7, 12, 13) and the existence of certain genetic and chromosomic arrangements (such as jumping genes and multigene families (14)) may facilitate the occurrence of functional mutations, thus easing the evolutionary process (7, 14). These traits are different from the classical adaptive characters, which relate to the capacity to perform specific interactions. The increased capacity of genetic recombination relates rather to the capacity to change (or to evolve) and is more strongly selectetd for in conditions of continued environmental change (7, 14). It is argued that it may make no difference for the individual whether it has or not these genetic traits. However, a group of species bearing them is at an advantage over groups or species lacking the trait, since there are more opportunities to produce advantageous variants (7, 14). This approach fails to explain how groups (or species) acquired the trait in the first place. The usual answer is that it has been acquired by chance. Furthermore, it has some difficulties to meet Sober’s criteria for group properties (9). It is difficult to see if these traits are any more group or species properties than, say, genes for a long neck in the case of the giraffe. I suggest that the explanation of the capacity for genetic recombination does not lie in group or species selection. Instead, I will argue that this trait confers advantage to genetic lineages. Suppose that an individual carries a jumping gene that has produced a lucky recombination event that in turn has conferred a better performance to the individual. This subject will be eventually more successful at reproducing. There is no doubt that in this case the selected properties are expressed at the individual level. It makes no real difference whether the mutation was caused by a jumping gene or some other agent. However, if successful mutations tend to occur again and again in the lineage of this individual, then its lineage will be favoured in a variety of circumstances. In every mutational instance, individual properties produce survival, but it is the capacity to produce useful mutations that becomes selected in the long run. This capacity is a property of the lineage and is caused by the presence of jumping genes in this case. In Hull’s terms (10) the selected replicator would be the jumping gene while the interactor would be the lineage of individuals. I propose to call this process lineage selection. An alternative possibility is to consider the jumping gene as both a relicator and an interactor, whose performance in producing useful mutations is the se-
MEDICAL llYF’OTHE8E.S
lected property. However, in each instance, selection occurs based on the properties of individuals and for each of these cases the individual may be considered as the interactor. Lineage selection is a consequence of the iteration of individual selection, however, selecting different properties at each time. In other words, without making a difference in individual performance, jumping genes could not be selected for. Lineage selection may be confused with group or species selection because these concepts usually imply reproductive interactions between individuals (2). However, from what I have argued, if a single individual carries the character it may still spread to the whole population or species because of its adaptive value. Therefore, group selection is clearly not necessary to spread the character. Furthermore, I have proposed that there is no group property that is necessarily produced by the possession of recombinatory characters. Instead, this appears as a property of the lineage. Finally, lineage selection may permit a much faster evolutionary rate than group of species selection, thus explaining the relatively rapid origin of some complex multigene systems. This has been claimed to be difficult to account for within the framework of group or species selection (14). References 1. Aboitiz F. Behavior, archetypes and the irreversibility of evolution. Medical Hypotheses 30: 87. 1989. 2. Eldredge N. Macroevolutionary Dynamics. McGraw Hill, New York, 1989. 3. Wynne-Edwards VC. Animal Dispersion in Relation to Social Behavior. Oliver and Boyd, Edinburgh, 1962. 4. Wvnne-Edwards VC. Evolution Throueh G~OUD Selection. ” a Blackwell Eds., London, 1986. 5. Wilson DS. A theory of group selection. Proceedings of the National Academy of Sciences (USA) 72: 143, 1975. 6. Gould SJ, Eldredge N. Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3: 115, 1977. 7. Stanley SM. Macroevolution. Pattern and Proces. Freeman and Company, San Francisco, 1979. 8. Van Valen L. Group selection and the evolution of dispersal. Evolution 25: 591, 1971. 9. Sober E. The Nature of Selection. Evolutionary Theory in Philosophical Focus. MIT Press, Cambridge, 1984. 10. Hull D. Interactors versus vehicles. pl9 ht The Role of Behavior in Evolution (HC Plotkin. ed.)., MIT Press. Cambridee.Y . 1988. 11. Dawkins R. The Selfish Gene. Oxford Press, Oxford, 1976. 12. Maynard Smith I. The Evolution of Sex. Cambridge Press, Cambridge, 1978. 13. Margulis L. Sagan D. Origins of Sex. Yale Press, New Haven, 1986. 14. Wills C. The Wisdom of the Genes. Basic Books, New York, 1989.