The Role of Mate Choice in Biocomputation: Sexual Selection as a Process of Search, Optimization and Diversification

The most successful, complex, and numerous species on earth are composed of sexually-reproducing animals and flowering plants. Both groups typically undergo a form of sexual selection through mate choice: animals are selected by conspecifics and flowering plants are selected by heterospecific pollinators. This suggests that the evolution of phenotypic complexity and diversity may be driven not simply by natural-selective adaptation to econiches, but by subtle interactions between natural selection and sexual selection. This paper reviews several theoretical arguments and simulation results in support of this view. Biological interest in sexual selection has exploded in the last 15 years (see Andersson, 1994; Cronin, 1991), but has not yet been integrated with the biocomputational perspective on evolution as a process of search and optimization (Holland, 1975; Goldberg, 1989). In the terminology of sexual selection theory, mate preferences for ‘viability indicators’ (e.g. Hamilton & Zuk, 1982) may enhance evolutionary optimization, and mate preferences for ‘aesthetic displays’ (e.g. Fisher, 1930) may enhance evolutionary search and diversification. Specifically, as a short-term optimization process, sexual selection can: (1) speed evolution by increasing the accuracy of the mapping from phenotype to fitness and thereby decreasing the ‘noise’ or ‘sampling error’ characteristic of many forms of natural selection, and (2) speed evolution by increasing the effective reproductive variance in a population even when survival-relevant differences are minimal, thereby imposing an automatic, emergent form of ‘fitness scaling’, as used in genetic algorithm optimization methods (see Goldberg, 1989). As a longer-term search process, sexual selection can: (3) help populations escape from local ecological optima, essentially by replacing genetic drift in Wright's (1932) “shifting balance” model with a much more powerful and directional stochastic process, and (4) facilitate the emergence of complex innovations, some of which may eventually show some ecological utility. Finally, as a process of diversification, sexual selection can (5) promote spontaneous sympatric speciation through assortative mating, increasing biodiversity and thereby increasing the number of reproductively isolated lineages performing parallel evolutionary searches (Todd & Miller, 1991) through an adaptive landscape. The net result of these last three effects is that sexual selection may be to macroevolution what genetic mutation is to microevolution: the prime source of potentially adaptive heritable variation, at both the individual and species levels. Thus, if evolution is understood as a biocomputational process of search, optimization, and diversification, sexual selection can play an important role complementary to that of natural selection. In that role, sexual selection may help explain precisely those phenomena that natural selection finds troubling, such as the success of sexually-reproducing lineages, the speed and robustness of evolutionary adaptation, and the origin of otherwise puzzling evolutionary innovations, such as the human brain (Miller, 1993). Implications of this view will be discussed for biology, psychology, and evolutionary approaches to artificial intelligence and robotics.

[1]  UDO M. SAVALLI,et al.  Female choice , 1989, Nature.

[2]  N. Eldredge Macroevolutionary Dynamics: Species, Niches, and Adaptive Peaks , 1989 .

[3]  J. Huxley Evolution: The Modern Synthesis , 1943 .

[4]  Yoh Iwasa,et al.  THE EVOLUTION OF COSTLY MATE PREFERENCES I. FISHER AND BIASED MUTATION , 1991, Evolution; international journal of organic evolution.

[5]  M. Wilson The ant and the peacock: altruism and sexual selection from darwin to today , 1992 .

[6]  A. Pomiankowski The costs of choice in sexual selection. , 1987, Journal of theoretical biology.

[7]  Lashon B. Booker,et al.  Proceedings of the fourth international conference on Genetic algorithms , 1991 .

[8]  A. Wilson,et al.  Birds, behavior, and anatomical evolution. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Brian K. Sullivan Passive and active female choice: A comment , 1989, Animal Behaviour.

[10]  F J Ayala,et al.  Tempo and mode in evolution. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Stewart W. Wilson,et al.  Environment structure and adaptive behavior from the ground up , 1993 .

[12]  G. A. Horridge,et al.  Animal species and evolution. , 1964 .

[13]  M. Ryan,et al.  Neuroanatomy influences speciation rates among anurans. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Andrew Pomiankowski,et al.  The evolution of female mating preferences for male genetic quality , 1988 .

[15]  Ernst Mayr,et al.  The emergence of evolutionary novelties , 1976 .

[16]  Charles Darwin,et al.  The movements and habits of climbing plants, by Charles Darwin. , 1876 .

[17]  E. Vrba,et al.  Macroevolutionary Trends: New Perspectives on the Roles of Adaptation and Incidental Effect , 1983, Science.

[18]  Robert D. Montgomerie Insects and Flowers: the Biology of a Partnership. Princeton University Press, Princeton, New Jersey (1985), ix, translated by M. A. Biederman-Thorson, +297. Price $35.00 , 1986 .

[19]  J M Thoday,et al.  Disruptive selection. , 1972, Proceedings of the Royal Society of London. Series B, Biological sciences.

[20]  B. Ratcliff,et al.  Development as an Evolutionary Process , 1987, The Yale Journal of Biology and Medicine.

[21]  M. Petrie,et al.  Peacocks with low mating success are more likely to suffer predation , 1992, Animal Behaviour.

[22]  S. A. Barnett,et al.  The major features of evolution , 1955 .

[23]  M. Ryan Sexual selection, sensory systems and sensory exploitation. , 1990 .

[24]  M. Enquist,et al.  Selection of exaggerated male traits by female aesthetic senses , 1993, Nature.

[25]  J T Manning,et al.  Fluctuating asymmetry, sexual selection and canine teeth in primates , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  C. LLOYD MORGAN,et al.  Natural Selection and Elimination , 1888, Nature.

[27]  George John Romanes Darwin, and after Darwin: An exposition of the Darwinian theory and a discussion of post-Darwinian questions: Post-Darwinian questions of heredity and utility, Vol. II, 2nd ed. , 1897 .

[28]  P. Simons,et al.  The action plant : movement and nervous behaviour in plants , 1992 .

[29]  E. Mayr Systematics and the Origin of Species , 1942 .

[30]  E. B. P. Darwin, and after Darwin , 1898, Nature.

[31]  Frederick S. Szalay,et al.  Evolution of permanent estrus displays in hominids , 1991 .

[32]  Mae-Wan Ho,et al.  Evolutionary Processes and Metaphors. , 1989 .

[33]  P. Pye-Smith The Descent of Man, and Selection in Relation to Sex , 1871, Nature.

[34]  A. Møller,et al.  Patterns of fluctuating asymmetry in avian feather ornaments: implications for models of sexual selection , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  T. Dobzhansky Genetics and the Origin of Species , 1937 .

[36]  Randy Thornhill,et al.  Fluctuating asymmetry and the mating system of the Japanese scorpionfly, Panorpa japonica , 1992, Animal Behaviour.

[37]  Charles Darwin,et al.  On the origin of species, 1859 , 1988 .

[38]  R. Lande,et al.  SEXUAL DIMORPHISM, SEXUAL SELECTION, AND ADAPTATION IN POLYGENIC CHARACTERS , 1980, Evolution; international journal of organic evolution.

[39]  M. Ryan,et al.  Directional Patterns of Female Mate Choice and the Role of Sensory Biases , 1992, The American Naturalist.

[40]  Karel F. Liem,et al.  Evolutionary Strategies and Morphological Innovations: Cichlid Pharyngeal Jaws , 1973 .

[41]  Masatoshi Nei,et al.  Evolution of genes and proteins. , 1983 .

[42]  M. Kirkpatrick SEXUAL SELECTION AND THE EVOLUTION OF FEMALE CHOICE , 1982, Evolution; international journal of organic evolution.

[43]  R A Fisher,et al.  The evolution of sexual preference. , 1915, The Eugenics review.

[44]  Charles E. Taylor,et al.  Artificial Life II , 1991 .

[45]  G. Beer,et al.  Evolution. Essays on aspects of evolutionary biology. , 1938 .

[46]  Geoffrey E. Hinton,et al.  How Learning Can Guide Evolution , 1996, Complex Syst..

[47]  W. Barker Ontogeny and phylogeny. , 1980, Archives of surgery.

[48]  M. Petrie,et al.  Peahens prefer peacocks with elaborate trains , 1991, Animal Behaviour.

[49]  S. Gould,et al.  Punctuated equilibria: an alternative to phyletic gradualism , 1972 .

[50]  Peter M. Todd,et al.  Parental Guidance Suggested: How Parental Imprinting Evolves Through Sexual Selection as an Adaptive Learning Mechanism , 1993, Adapt. Behav..

[51]  Donald A. Dewsbury,et al.  Effects of novelty of copulatory behavior: The Coolidge effect and related phenomena. , 1981 .

[52]  P. Feldman Evolution of sex , 1975, Nature.

[53]  Stuart A. Kauffman,et al.  The origins of order , 1993 .

[54]  Niles Eldredge,et al.  Information, Economics, and Evolution , 1986 .

[55]  L. V. Valen,et al.  A STUDY OF FLUCTUATING ASYMMETRY , 1962 .

[56]  N. Burley,et al.  Mate choice in plants: tactics, mechanisms and consequences. , 1983 .

[57]  G. C. Williams Sex and evolution. , 1975, Monographs in population biology.

[58]  J. Haldane,et al.  The Causes of Evolution , 1933 .

[59]  Dario Floreano,et al.  From Animals to Animats 2: Proceedings of the Second International Conference on Simulation of Adaptive Behavior , 2000, Journal of Cognitive Neuroscience.

[60]  Hilla Peretz,et al.  The , 1966 .

[61]  Hepsa Ely,et al.  The Material Basis of Evolution , 1915, Nature.

[62]  M. Eigen,et al.  Steps Towards Life: A Perspective on Evolution , 1992 .

[63]  J. W. Bradbury Sexual Selection: Testing the Alternatives , 1987 .

[64]  J. M. Thoday,et al.  Review Lecture Disruptive selection , 1972, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[65]  Sewall Wright,et al.  CHARACTER CHANGE, SPECIATION, AND THE HIGHER TAXA , 1982, Evolution; international journal of organic evolution.

[66]  J. Endler Signals, Signal Conditions, and the Direction of Evolution , 1992, The American Naturalist.

[67]  Julian Huxley,et al.  Evolution as a Process , 1958 .

[68]  T. Cockerell,et al.  Genetics and the Origin of Species , 1937 .

[69]  W. Eberhard,et al.  SPECIES ISOLATION, GENITAL MECHANICS, AND THE EVOLUTION OF SPECIES‐SPECIFIC GENITALIA IN THREE SPECIES OF MACRODACTYLUS BEETLES (COLEOPTERA, SCARABEIDAE, MELOLONTHINAE) , 1992, Evolution; international journal of organic evolution.

[70]  Jon Marks,et al.  Development as an evolutionary process: Edited by Rudolf A. Raff & Elizabeth C. Raff (1987) New York: Alan R. Liss, Inc. xiv and 329 pp. ISBN 0-8451-2207-X. $58.00 , 1987 .

[71]  Inman Harvey,et al.  Genetic Convergence in a Species of Evolved Robot Control Architectures , 1993, ICGA.

[72]  Jack L Crosby,et al.  The evolution of genetic discontinuity: Computer models of the selection of barriers to interbreeding between subspecies , 1970, Heredity.

[73]  Frank K. McKinney Multidisciplinary perspectives on evolutionary innovations , 1988 .

[74]  H. H. Swinnerton Development and Evolution , 1938, Nature.

[75]  H. Roitblat,et al.  Evolutionary wanderlust : Sexual selection with directional mate preferences , 1993 .

[76]  L. V. Valen,et al.  ADAPTIVE ZONES AND THE ORDERS OF MAMMALS. , 1971 .

[77]  M. Kimura,et al.  The neutral theory of molecular evolution. , 1983, Scientific American.

[78]  John Tyler Bonner,et al.  Evolution and Development , 1998 .

[79]  Robert M. May,et al.  How Many Species Inhabit the Earth , 1992 .

[80]  Richard Dawkins,et al.  The eye in a twinkling , 1994, Nature.

[81]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[82]  A. Rowell,et al.  Models in Paleobiology , 1973 .

[83]  B. Clarke The evidence for apostatic selection , 1969, Heredity.

[84]  T. Guilford,et al.  Receiver psychology and the evolution of animal signals , 1991, Animal Behaviour.

[85]  Andrew Pomiankowski,et al.  How to find the top male , 1990, Nature.

[86]  T. Schopf Models in Paleobiology , 1972 .

[87]  R. Lande Models of speciation by sexual selection on polygenic traits. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[88]  John Maynard Smith,et al.  When learning guides evolution , 1987, Nature.

[89]  E. Vrba Environment and evolution: alternative causes of the temporal distribution of evolutionary events , 1985 .

[90]  A. Zahavi Mate selection-a selection for a handicap. , 1975, Journal of theoretical biology.

[91]  Inman Harvey,et al.  Evolving visually guided robots , 1993 .

[92]  Stephen Jay Gould,et al.  The hierarchical expansion of sorting and selection: sorting and selection cannot be equated , 1986, Paleobiology.

[93]  P. Schuster,et al.  Stationary mutant distributions and evolutionary optimization. , 1988, Bulletin of mathematical biology.

[94]  David Pimentel,et al.  A Population Model of Sympatric Speciation , 1967, The American Naturalist.

[95]  C. Darwin The Movements and Habits of Climbing Plants , 1875, Nature.

[96]  Y. Iwasa,et al.  THE EVOLUTION OF COSTLY MATE PREFERENCES II. THE “HANDICAP” PRINCIPLE , 1991, Evolution; international journal of organic evolution.

[97]  N. Pierce Origin of Species , 1914, Nature.

[98]  Robert M. May,et al.  How many species , 1990 .

[99]  L. V. Van Valen,et al.  ADAPTIVE ZONES AND THE ORDERS OF MAMMALS , 1971, Evolution; international journal of organic evolution.

[100]  N. Eldredge Unfinished Synthesis: Biological Hierarchies and Modern Evolutionary Thought , 1985 .

[101]  Inman Harvey,et al.  Issues in evolutionary robotics , 1993 .

[102]  Peter M. Todd,et al.  On the Sympatric Origin of Species: Mercurial Mating in the Quicksilver Model , 1991, ICGA.

[103]  James D. Murray,et al.  Genetic and ecological diversity: The sport of nature , 1991 .

[104]  P. O'donald Genetic Models of Sexual Selection , 1980 .

[105]  J. McKeen Cattell "Darwin, and after Darwin. II. Post-Darwinian Questions; Heredity and Utility" and "The Primary Factors of Organic Evolution." , 1896 .

[106]  Geoffrey F. Miller,et al.  Exploiting Mate Choice in Evolutionary Computation: Sexual Selection as a Process of Search, Optimization, And Diversification , 1994, Evolutionary Computing, AISB Workshop.

[107]  W. Eberhard,et al.  COPULATORY COURTSHIP AND CRYPTIC FEMALE CHOICE IN INSECTS , 1991 .