Relative Importance Of Natural Selection Research Articles

Mutator genomes decay, despite sustained fitness gains, in a long-term experiment with bacteria

Understanding the extreme variation among bacterial genomes remains an unsolved challenge in evolutionary biology, despite long-standing debate about the relative importance of natural selection, mutation, and random drift. A potentially important confounding factor is the variation in mutation rates between lineages and over evolutionary history, which has been documented in several species. Mutation accumulation experiments have shown that hypermutability can erode genomes over short timescales. These results, however, were obtained under conditions of extremely weak selection, casting doubt on their general relevance. Here, we circumvent this limitation by analyzing genomes from mutator populations that arose during a long-term experiment with Escherichia coli, in which populations have been adaptively evolving for >50,000 generations. We develop an analytical framework to quantify the relative contributions of mutation and selection in shaping genomic characteristics, and we validate it using genomes evolved under regimes of high mutation rates with weak selection (mutation accumulation experiments) and low mutation rates with strong selection (natural isolates). Our results show that, despite sustained adaptive evolution in the long-term experiment, the signature of selection is much weaker than that of mutational biases in mutator genomes. This finding suggests that relatively brief periods of hypermutability can play an outsized role in shaping extant bacterial genomes. Overall, these results highlight the importance of genomic draft, in which strong linkage limits the ability of selection to purge deleterious mutations. These insights are also relevant to other biological systems evolving under strong linkage and high mutation rates, including viruses and cancer cells.

Lineage isolation in the face of active gene flow in the coastal plant wild radish is reinforced by differentiated vernalisation responses.

BackgroundThe respective role and relative importance of natural selection and gene flow in the process of population divergence has been a central theme in the speciation literature. A previous study presented conclusive evidence that wild radish on Japanese islands comprises two genetically isolated lineages: the southern and northern groups. However, a general understanding of the lineage isolation with frequent seed flow of the coastal plant species is still unclear. We surveyed nucleotide polymorphisms over 14 nuclear loci in 72 individuals across the Japan–Ryukyu Islands Arc to address the demographic history of wild radish utilising the isolation-with-migration (IM) model. In addition, we investigated the flowering times of individuals in different wild radish lineages, with and without cold exposure, to assess their respective vernalisation responses.ResultsCoalescent simulations suggested that divergence between the southern and northern lineages of wild radish began ~18,000 years ago, initially during the Last Glacial Maximum (LGM) period. The gene flow from the southern to northern groups was considerably higher than that in the opposite direction, indicating effective dispersal of viable seeds via the northward Kuroshio Current. Our greenhouse experiments indicated that cold exposure was not required for flowering in the southern group, but could advance the date of flowering, suggesting that vernalisation would be facultative in the southern group. In contrast, the northern group was either unable to flower or flowered later without prior cold exposure, and thus had an obligate requirement for cold treatment.ConclusionsThe south–north lineage divergence in wild radish could be triggered by a directional change in the sea current during the ice age, despite gene flow due to the high dispersability and longevity of seeds. We also found that temperature profoundly affected the vernalisation responses of wild radish, which may repress reproductive success and ultimately drive and reinforce intra-specific differentiation between the two lineages of wild radish. This study provides new insights into the maintenance of lineage differentiation with on-going gene flow in coastal plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0655-7) contains supplementary material, which is available to authorized users.

Natural selection in a postglacial range expansion: the case of the colour cline in the European barn owl.

Gradients of variation--or clines--have always intrigued biologists. Classically, they have been interpreted as the outcomes of antagonistic interactions between selection and gene flow. Alternatively, clines may also establish neutrally with isolation by distance (IBD) or secondary contact between previously isolated populations. The relative importance of natural selection and these two neutral processes in the establishment of clinal variation can be tested by comparing genetic differentiation at neutral genetic markers and at the studied trait. A third neutral process, surfing of a newly arisen mutation during the colonization of a new habitat, is more difficult to test. Here, we designed a spatially explicit approximate Bayesian computation (ABC) simulation framework to evaluate whether the strong cline in the genetically based reddish coloration observed in the European barn owl (Tyto alba) arose as a by-product of a range expansion or whether selection has to be invoked to explain this colour cline, for which we have previously ruled out the actions of IBD or secondary contact. Using ABC simulations and genetic data on 390 individuals from 20 locations genotyped at 22 microsatellites loci, we first determined how barn owls colonized Europe after the last glaciation. Using these results in new simulations on the evolution of the colour phenotype, and assuming various genetic architectures for the colour trait, we demonstrate that the observed colour cline cannot be due to the surfing of a neutral mutation. Taking advantage of spatially explicit ABC, which proved to be a powerful method to disentangle the respective roles of selection and drift in range expansions, we conclude that the formation of the colour cline observed in the barn owl must be due to natural selection.

Imperfect morphological convergence: variable changes in cranial structures underlie transitions to durophagy in moray eels.

Convergence is central to the study of evolution because it demonstrates the power of natural selection to deterministically shape phenotypic diversity. However, the conditions under which a common morphology repeatedly evolves may be restrictive. Many factors, such as differing genetic and environmental backgrounds and many-to-one mapping of form to function, contribute to variability in responses to selection. Nevertheless, lineages may evolve similar, even if not identical, forms given a shared selective regime, providing opportunities to examine the relative importance of natural selection, constraint, and contingency. Here, we show that following 10 transitions to durophagy (eating hard-shelled prey) in moray eels (Muraenidae), cranial morphology repeatedly evolved toward a novel region of morphological space indicative of enhanced feeding performance on hard prey. Disparity among the resulting 15 durophagous species, however, is greater than disparity among ancestors that fed on large evasive prey, contradicting the pattern expected under convergence. This elevated disparity is a consequence of lineage-specific responses to durophagy, in which independent transitions vary in the suites of traits exhibiting the largest changes. Our results reveal a pattern of imperfect convergence, which suggests shared selection may actually promote diversification because lineages often differ in their phenotypic responses to similar selective demands.

A guide to the genomics of ecological speciation in natural animal populations

Interest in ecological speciation is growing, as evidence accumulates showing that natural selection can lead to rapid divergence between subpopulations. However, whether and how ecological divergence can lead to the buildup of reproductive isolation remains under debate. What is the relative importance of natural selection vs. neutral processes? How does adaptation generate reproductive isolation? Can ecological speciation occur despite homogenizing gene flow? These questions can be addressed using genomic approaches, and with the rapid development of genomic technology, will become more answerable in studies of wild populations than ever before. In this article, we identify open questions in ecological speciation theory and suggest useful genomic methods for addressing these questions in natural animal populations. We aim to provide a practical guide for ecologists interested in incorporating genomic methods into their research programs. An increased integration between ecological research and genomics has the potential to shed novel light on the origin of species.

Viviparity‐driven Conflict

Equipped with Mendel's laws and only rudimentary knowledge of genes and genomes, the architects of the Modern Synthesis provided key insights into the dynamics of gene frequency change within populations. Extension of population genetic models to speciation identified Dobzhansky-Muller incompatibilities (negative epistatic interactions between genes from isolated populations) as the primary cause of hybrid inviability and sterility, a view consistent with empirical findings on the genetics of reproductive isolation in Drosophila. Although speciation models have become increasingly mathematically sophisticated, many remain based on an overly static concept of the genome, grounded in Mendelian genetics and devoid of potentially important biological details. A unifying theory of speciation therefore remains elusive, with debate over the relative importance of natural selection, sexual selection, sexual conflict, genetic drift, and selfish genetic elements in the evolution of reproductive isolation. Drawing on recent findings in molecular genetics and comparative genomics, we revisit, update, and extend the theory that reproductive mode plays a crucial role in shaping the speciation process. By providing a direct conduit for manipulation of the mother's physiology by genes expressed in the embryo, viviparity creates a postfertilization arena for genomic conflicts absent in species that lay eggs. In polyandrous species, viviparity-driven conflict (VDC) is likely to generate perpetual antagonistic coevolution between genes expressed during embryonic development and those involved in maternal reproductive physiology, thereby accelerating the rate at which postzygotic isolation evolves between populations. Moreover, in mammals and flowering plants, VDC has favored the evolution of genomic imprinting and a central role for epigenetic mechanisms in the regulation of antagonistic patterns of gene expression by maternally and paternally inherited genomes. VDC can account for the rapid rate at which mammals and viviparous fishes lose their ability to hybridize; the key role of the triploid endosperm in postzygotic reproductive isolation in flowering plants; and the kinds of traits, genes, and gene regulatory systems most critical to the evolution of postzygotic reproductive isolation in live-bearing species.

Island selection on mammalian life-histories: genetic differentiation in offspring size

BackgroundSince Darwin's pioneering work, evolutionary changes in isolated island populations of vertebrates have continued to provide the strongest evidence for the theory of natural selection. Besides macro-evolutionary changes, micro-evolutionary changes and the relative importance of natural selection vs. genetic drift are under intense investigation. Our study focuses on the genetic differentiation in morphological and life-history traits in insular populations of a small mammal the bank vole Myodes glareolus.ResultsOur results do not support the earlier findings for larger adult size or lower reproductive effort in insular populations of small mammals. However, the individuals living on islands produced larger offspring than individuals living on the mainland. Genetic differentiation in offspring size was further confirmed by the analyses of quantitative genetics in lab. In insular populations, genetic differentiation in offspring size simultaneously decreases the additive genetic variation (VA) for that trait. Furthermore, our analyses of differentiation in neutral marker loci (Fst) indicate that VA is less than expected on the basis of genetic drift alone, and thus, a lower VA in insular populations could be caused by natural selection.ConclusionWe believe that different selection pressures (e.g. higher intraspecific competition) in an insular environment might favour larger offspring size in small mammals. Island selection for larger offspring could be the preliminary mechanism in a process which could eventually lead to a smaller litter size and lower reproductive effort frequently found in insular vertebrates.

SPATIAL DIFFERENTIATION FOR FLOWER COLOR IN THE DESERT ANNUAL LINANTHUS PARRYAE: WAS WRIGHT RIGHT?

Understanding the evolutionary mechanisms that contribute to the local genetic differentiation of populations is a major goal of evolutionary biology, and debate continues regarding the relative importance of natural selection and random genetic drift to population differentiation. The desert plant Linanthus parryae has played a prominent role in these debates, with nearly six decades of empirical and theoretical work into the causes of spatial differentiation for flower color. Plants produce either blue or white flowers, and local populations often differ greatly in the frequencies of the two color morphs. Sewall Wright first applied his model of "isolation by distance" to investigate spatial patterns of flower color in Linanthus. He concluded that the distribution of flower color morphs was due to random genetic drift, and that Linanthus provided an example of his shifting balance theory of evolution. Our results from comprehensive field studies do not support this view. We studied an area in which flower color changed abruptly from all-blue to all-white across a shallow ravine. Allozyme markers sampled across these regions showed no evidence of spatial differentiation, reciprocal transplant experiments revealed natural selection favoring the resident morph, and soils and the dominant members of the plant community differed between regions. These results support the hypothesis that local differences in flower color are due to natural selection, not due to genetic drift.

CONTRASTING PATTERNS OF QUANTITATIVE AND NEUTRAL GENETIC VARIATION IN LOCALLY ADAPTED POPULATIONS OF THE NATTERJACK TOAD, BUFO CALAMITA

The relative importance of natural selection and genetic drift in determining patterns of phenotypic diversity observed in nature is still unclear. The natterjack toad (Bufo calamita) is one of a few amphibian species capable of breeding in saline ponds, even though water salinity represents a considerable stress for them. Results from two common-garden experiments showed a pattern of geographic variation in embryonic salinity tolerance among populations from either fresh or brackish environments, consistent with the hypothesis of local adaptation. Full-sib analysis showed increased variation in survival among sibships within population for all populations as osmotic stress was increased (broad-sense heritability increased as salinity raised). Nevertheless, toads native to the brackish water environment had the highest overall survival under brackish conditions. Levels of population genetic differentiation for salinity tolerance were higher than those of neutral genetic differentiation, the latter obtained through the analysis of eight microsatellite loci. Microsatellite markers also revealed little population differentiation, lack of an isolation-by-distance pattern, and moderate gene flow connecting the populations. Therefore, environmental stress tolerance appears to have evolved in absence of geographic isolation, and consequently we reject the null hypothesis of neutral differentiation.

Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys?

A central controversy among biologists is the relative importance of natural selection and genetic drift as creative forces shaping biological diversification (Fisher 1930; Wright 1931). Historically, this controversy has been an effective engine powering several evolutionary research programs during the last century (Provine 1989). While all biologists agree that both processes operate in nature to produce evolutionary change, there is a diversity of opinion about which process dominates at any particular organizational level (from DNA and proteins to complex morphologies). To address this last level, we did a broadscale analysis of cranial diversification among all living New World monkeys. Quantitative genetic models yield specific predictions about the relationship between variation patterns within and between populations that may be used to test the hypothesis that genetic drift is a sufficient explanation for morphological diversification. Diversity at several levels in a hierarchy of taxonomic/phylogenetics relationship was examined from species within genera to families within superfamilies. The major conclusion is that genetic drift can be ruled out as the primary source of evolutionary diversification in cranial morphology among taxa at the level of the genus and above as well as for diversification of most genera. However, drift may account for diversification among species within some Neotropical primate genera, implying that morphological diversification associated with speciation need not be adaptive in some radiations.

CONTRASTING PATTERNS OF QUANTITATIVE AND NEUTRAL GENETIC VARIATION IN LOCALLY ADAPTED POPULATIONS OF THE NATTERJACK TOAD, BUFO CALAMITA

The relative importance of natural selection and genetic drift in determining patterns of phenotypic diversity observed in nature is still unclear. The natterjack toad (Bufo calamita) is one of a few amphibian species capable of breeding in saline ponds, even though water salinity represents a considerable stress for them. Results from two common-garden experiments showed a pattern of geographic variation in embryonic salinity tolerance among populations from either fresh or brackish environments, consistent with the hypothesis of local adaptation. Full-sib analysis showed increased variation in survival among sibships within population for all populations as osmotic stress was increased (broad-sense heritability increased as salinity raised). Nevertheless, toads native to the brackish water environment had the highest overall survival under brackish conditions. Levels of population genetic differentiation for salinity tolerance were higher than those of neutral genetic differentiation, the latter obtained through the analysis of eight microsatellite loci. Microsatellite markers also revealed little population differentiation, lack of an isolation-by-distance pattern, and moderate gene flow connecting the populations. Therefore, environmental stress tolerance appears to have evolved in absence of geographic isolation, and consequently we reject the null hypothesis of neutral differentiation.

Contemporary fisherian life-history evolution in small salmonid populations.

The relative importance of natural selection and random drift in phenotypic evolution has been discussed since the introduction of the first population genetic models. The empirical evidence used to evaluate the evolutionary theories of Fisher and Wright remains obscure because formal tests for neutral divergence or sensitive attempts to separate the effects of selection and drift are scarce, subject to error, and have not been interpreted in the light of well-known population demography. We combined quantitative genetic and microsatellite DNA analyses to investigate the determinants of contemporary life-history evolution in isolated populations of grayling (Thymallus thymallus, Salmonidae) that originated from a common source 80-120 years ago. Here we show that natural selection was the dominant diversifying agent in the evolution of the quantitative traits. However, the populations were founded by a small number of individuals, exhibit very low microsatellite-based effective sizes and show genetic imprints of severe 'bottlenecks'; which are conditions often suggested to constrain selection and favour drift. This study demonstrates a very clear case of fisherian evolution in small natural populations across a contemporary timescale.

The importance of phylogeny and ecology in microgeographical variation in the morphology of four Canarian species of Aeonium (Crassulaceae)

The relative importance of natural selection in the diversification of organisms can be assessed indirectly using matrix correspondence. The present study determines the environmental and genetic correlates of microgeographical variation in the growth form, leaf form and flower morphology in populations of four Aeonium species from section Leuconium using partial regression methods. The phylogeny of the four species and the other 12 species in the section was deduced from amplified fragment length polymorphism (AFLP). Pubescence of floral organs and flower size correlate with the phylogeny while traits related to growth form, leaf form, flower construction and inflorescence size correlate with ecological factors. The variation in the latter four traits may therefore reflect selection by current ecological conditions while variation in pubescence and flower size may reflect historical events like neutral mutations, founder events and drift. Additionally, the morphological analyses revealed a large amount of variation in all traits within populations. This suggests a possible influence of microhabitat on the variation in morphology of Aeonium in the Canary Islands.

Mexical plant phenology: is it similar to Mediterranean communities?

The sclerophyllous, evergreen vegetation found in Mexico under tropical climate is named ‘Mexical’ (MEX) and presents many traits that have been thought to converge under a Mediterranean climate. Flowering phenology is strongly similar across Mediterranean-type ecosystems (MTEs) and this paper investigates MEX plant phenology in this context. The common history of the vegetation and the differences in the climatic conditions experienced by MEX and MTE taxa provide an ideal scenario to infer the relative importance of natural selection and historical constraints in the phenological response of plants to climatic conditions. This study has involved collecting field and bibliographic data on flowering phenology of MEX communities to detect (1) similarities at the community level between MTEs and MEX, (2) similarities between Tertiary and Quaternary taxa in MTEs and MEX, and (3) similarities between congeneric taxa from MEX and MTEs (taxa sharing a common ancestor but having evolved under different climates). Flowering in MEX does not occur mainly in spring, as in MTEs, but in summer, suggesting a response that maximizes water use in the rainy season. Flowering phenology of MEX species differed from their MTE congeneric species, suggesting that even though a common ancestor is shared, environmental pressures have led to different phenological responses in MEX and MTE plants. The flowering season for species that originated in the Tertiary and Quaternary did not differ in MEX, as expected, because of climatic uniformity along the whole time line. In MTEs, flowering differences between Tertiary and Quaternary species were not congruent, suggesting that the balance between the historical constraints and the selective force of the Mediterranean climate is different among the three MTEs, and a particular explanation is needed for each. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 138, 297–303.

Urn Models, Replicator Processes, and Random Genetic Drift

To understand the relative importance of natural selection and random genetic drift in finite but growing populations, the asymptotic behavior of a class of generalized Polya urns is studied using the method of ordinary differential equation (ODE). Of particular interest is the replicator process: two balls (individuals) are chosen from an urn (the population) at random with replacement and balls of the same colors (strategies) are added or removed according to probabilities that depend only on the colors of the chosen balls. Under the assumption that the expected number of balls being added always exceeds the expected number of balls being removed whenever balls are in the urn, the probability of nonextinction is shown to be positive. On the event of nonextinction, three results are proven: (i) the number of balls increases asymptotically at a linear rate, (ii) the distribution x(n) of strategies at the nth update is a noisy Cauchy-Euler approximation to the mean limit ODE of the process, and (iii) the limit set of x(n) is almost surely a connected internally chain recurrent set for the mean limit ODE. Under a stronger set of assumptions, it is shown that for any attractor of the mean limit ODE there is a positive probability that the limit set for x(n) lies in this attractor. Theoretical and numerical estimates for the probabilities of nonextinction and convergence to an attractor suggest that random genetic drift is more likely to overcome natural selection in small populations for which pairwise interactions lead to highly variable outcomes, and is less likely to overcome natural selection in large populations with the potential for rapid growth.

Population dynamics and evolutionary processes: the manifold roles of habitat selection

Any character that has a substantial effect on a species' distribution and abundance can exert a variety of indirect effects on evolutionary processes. It is suggested that an organism's capacity for habitat selection is just such a character. Habitat selection can constrain the selective environment experienced by a population. Habitat selection can also indirectly influence the relative importance of natural selection, drift, and gene flow, through its effect on population size and growth rate. In many circumstances (but not all), habitat selection increases population size and growth rate, and thereby makes selection in a local environment more effective than drift and gene flow.

TEMPORAL STABILITY OF LACTATE DEHYDROGENASE-A CLINES OF THE HIGH COCKSCOMB, ANOPLARCHUS PURPURESCENS.

In marine species with planktonic larval stages, strong geographic differentiation among resident adult populations is noteworthy in that identification of the forces and mechanisms which create such local differentiation allows an assessment of the relative importance of natural selection in promoting genetic divergence. Williams et al. (1973), and later Koehn and Williams (1978), focused on this problem in their analysis of genetic differentiation in the American eel, Anguilla rostrata. Their study centered on the interaction between age-dependent differentiation (elvers vs. resident adults) and spatial differentiation of groups along a latitudinal transect. They found different patterns of differentiation which depended upon the specific genetic marker under analysis. At the Mdh locus, allele frequencies were homogeneous among age-groups and among localities, suggesting recruitment of elvers from a common zygotic pool with no subsequent divergence between groups of colonists in situ. In contrast, at the Sdh locus, they observed a significant spatial component of variation across latitude, but one which was equally pronounced in both age groups. This result suggested (in light of the life history of the American eel) that divergence occurred prior to larval recruitment and was not further accentuated in situ. Finally, at the Phi-II locus, they observed that allele frequencies of newly recruited larvae were uniform across the transect (once again suggesting a common zygotic pool), but that geographic differentiation of adults was significant. This latter pattern would be consistent with a predominant role of local selective factors in promoting genetic divergence and it suggested selection intensities of about 10% per generation. Although the power of their analysis lies largely in the peculiar migrational history of the American eel, there is no reason to believe that the differences in genetic composition between life stages observed by Williams et al. (1973) and Koehn and Williams (1978) are in any way unique to Anguilla. As they point out, it is reasonable to expect that age-specific selection would operate in other species with planktonic larvae, but similar analyses have been rarely conducted. Actually, the degree of geographic differentiation in the American eel is rather slight; for example, systematic variation in Phi-II allele frequencies is on the order of 5% per degree of latitude (Koehn and Williams, 1978). In other marine fishes with planktonic larvae, more pronounced examples of geographic variation are known. In Anoplarchus purpurescens, an intertidal blennioid fish of the northwestern Pacific Ocean, relatively sharp differences in allele frequency over short distances have been reported (Johnson, 1971, 1977; Sassaman and Yoshiyama, 1979; Yoshiyama and Sassaman, unpubl.). Here we explore temporal (age-group) aspects of allele-frequency variation along two pronounced gradients of gene-frequency change in Anoplarchus. Our analysis follows the same logical format of Williams et al. (1973) and Koehn and Williams (1978). In addition we examine yearto-year stability of these gene-frequency clines by reference to previously published information (Johnson, 1971; Sassaman and Yoshiyama, 1979) for the same sampling sites. Since the presumption of extensive

Pollinator behaviour and natural selection for flower colour in Delphinium nelsonii

Evolutionary biologists continue to disagree about the relative importance of natural selection, drift and phylogenetic constraint in determining characteristics of an organism1. Because of the difficulty of identifying examples of selection in nature there are few rigorous field studies of selection2–6. We have been studying selection on flower colour in the small perennial larkspur Delphinium nelsonii, a native to mountains of the western USA. Previously we showed that white-flowered forms, which are very rare in natural populations, produce fewer seeds than their common blue-flowered conspecifics, and that this selective disadvantage results from partial discrimination against white flowers by bumblebee and hummingbird pollinators7. Here we present evidence that discrimination occurs because white flowers have inferior ‘nectar guides’ and therefore require longer handling times than blue flowers. Pollinators may thus experience lower net rates of energy intake on white flowers, a sufficient reason for undervisitation by optimally-foraging animals.

Human evolution.

HUMAN EVOLUTION S. L. WASHBURN* Over the last 25 years there has been remarkable progress in a wide variety of sciences. The impact of the new methods and understandings has brought major changes to the study of human evolution. In a very few years the whole framework of space, time, and the fossil record has been modified. Even the synthetic theory, which seemed so secure a few years ago, is challenged by the neutral theory, and Dobzhansky, Ayala, Stebbins, et al. state that the relative importance of natural selection and stochastic factors "remains the most important unsolved problem in our understanding of the mechanisms that bring about biological evolution" [1, P- 164]. The purpose of this paper is to sketch these developments and to stress that, in my opinion, they are not minor. In one sense the new inevitably builds on the old, and those who do not know history are bound to repeat the errors of the past. But, in a different sense, those who rely too heavily on the past are bound to make the old mistakes. It has not been easy for students of human evolution to escape from the history of their subject. Even today people look to anatomy to settle the problems of evolution. Molecular biology offers far more powerful methods and shows why anatomy could not solve the problem of man's place in nature. The early theories of human evolution were based on comparative anatomy and embryology. Pilbeam has described these theories as "fossil free" [2, p. 7]. There were either no relevant fossils or so few that they exerted little influence on the theories. For example, scientists could not decide whether the original Neanderthal skeleton was a fossil or the remains of a pathological modern human. Major scientists were on both sides of the debate, and it was not until a number of skeletons were found around the turn of the century that most scientists accepted the The author thanks Alice Davis for editorial assistance and the Wenner-Gren Foundation for Anthropological Research for support. *Department of Anthropology, University of California, Berkeley, California 94720.© 1982 by The University of Chicago. AU rights reserved. 003 1 -5982/82/2504-0308$0 1 .00 Perspectives in Biology and Medicine, 25, 4 ¦ Summer 1982 583 Neanderthal as a kind of human being. Even then Neanderthals were described as "uncouth," "repellent," "unattractive," and incapable of fine coordination of the fingers: certainly belonging to a separate species [3]. Elliot Smith and Boule, who shared these views, were leaders in the scientific study of human evolution, and it was many years before Cave and Straus [4] showed that the basic descriptions of the bones had been grossly distorted by the opinions of those describing them. The image of Neanderthal presented to the general public and repeated in book after book was far removed from the actual study of the bones, and it was the image of a primitive, unattractive, and undesirable creature that created the interest in Neanderthal. Hrdlicka's [5] calm description of "the Neanderthal phase of man" could not compete with Boule's dramatic reconstruction. The "fossils" of the 1920s were an odd lot. They included (and I am only considering specimens accepted by major scientists) genuine fossils, mistakes, fragments, fakes, and gross misconstructions. If the early studies had been "fossil free," they were followed by studies which were "nonsense rich." The most careful scientists could not tell which fossils were genuine and well enough preserved to be useful and which were simply misleading. The nonsense-rich era produced futile and often acrimonious debate. In our culture it is customary, when looking back, to consider who was right and who was wrong. Both the fossil-free and the nonsense-rich eras produced theories which were stoutly defended and can only be understood in terms of opinions of times long past. For example, how could anyone accept Piltdown, a modern braincase with an ape'sjaw? This seems impossible today, but wise scientists (Keith and Hooton) accepted it, and other wise scientists (Hrdlicka and Weidenreich) did not. Personal wisdom and scientific training were not enough to lead to useful debate, and the opinions of others were usually dismissed...

NATURAL SELECTION AND RANDOM GENETIC DRIFT IN PHENOTYPIC EVOLUTION.

In discussions of the major features of evolution, Simpson (1953) applied population genetic models to the interpretation of the fossil record. Most population genetics theory concentrates on details of the genetic system, such as gene frequencies and recombination rates, which cannot be directly observed or inferred from measurements on polygenic characters. Analysis of phenotypic data, particularly fossil material, requires models which are framed as much as possible in phenotypic terms. Starting from a simple formula of quantitative genetics, the methods of population genetics are used here to make a theory of the evolution of the average phenotype in a population by natural selection and random genetic drift. By analogy with Wright's (1931) adaptive topography for genotypes, Simpson (1953) proposed the concept of adaptive zones for phenotypes. This is an intuitive method of visualizing the dynamics of phenotypic evolution in terms of the degree of adaptation of the various phenotypes in a population, it usually being thought that natural selection increases adaptation. Such qualitative ideas are used by most evolutionary biologists and the notion of adaptive zones is popular among paleontologists. In the present paper, the concept of adaptive zones is clarified by the construction of an adaptive topography for the average phenotype in a population. This shows that with constant fitnesses the average phenotype evolves toward the nearest adaptive zone in the phenotype space. But if fitnesses are frequency-dependent the average phenotype may evolve away from an adaptive zone. A method is developed for estimating the minimum selective mortality necessary to produce an observed rate of evolution. In examples of the evolution of tooth characters in Tertiary mammals, these minimum selective mortalities are found to be exceedingly small. In his paper on the measurement of rates of evolution, Haldane (1949) stated that slowness of the rate of change makes it clear that agencies other than natural selection cannot be neglected because they are extremely slow by laboratory standards or even undetectable during a human lifetime. He briefly discussed mutation pressure. Random genetic drift due to finite population size is another such agency. The relative importance of natural selection and random genetic drift has been debated since Wright (1931, 1932) proposed that evolution is a stochastic process. Fisher (1958), for example, believed that random genetic drift is insignificant in relation to natural selection. The debate continues today at a more biochemical level (Lewontin, 1974). In order to objectively evaluate the role of random genetic drift in macro-evolutionary events, it is necessary to use mathematical models to determine the rate of evolution which can occur by repeated samplings of genetic material in a finite population. This paper presents a statistical test for the hypothesis of evolution by random genetic drift, contingent on the effective population size. In examples from the fossil record, it is found that rates of evolution equal to or greater than those observed have a significant probability of occurring by random genetic drift