Post by Admin on Jun 20, 2020 19:21:26 GMT
Biological Races in Humans
Alan R. Templeton
Abstract
Races may exist in humans in a cultural sense, but biological concepts of race are needed to access their reality in a non-species-specific manner and to see if cultural categories correspond to biological categories within humans. Modern biological concepts of race can be implemented objectively with molecular genetic data through hypothesis-testing. Genetic data sets are used to see if biological races exist in humans and in our closest evolutionary relative, the chimpanzee. Using the two most commonly used biological concepts of race, chimpanzees are indeed subdivided into races but humans are not. Adaptive traits, such as skin color, have frequently been used to define races in humans, but such adaptive traits reflect the underlying environmental factor to which they are adaptive and not overall genetic differentiation, and different adaptive traits define discordant groups. There are no objective criteria for choosing one adaptive trait over another to define race. As a consequence, adaptive traits do not define races in humans. Much of the recent scientific literature on human evolution portrays human populations as separate branches on an evolutionary tree. A tree-like structure among humans has been falsified whenever tested, so this practice is scientifically indefensible. It is also socially irresponsible as these pictorial representations of human evolution have more impact on the general public than nuanced phrases in the text of a scientific paper. Humans have much genetic diversity, but the vast majority of this diversity reflects individual uniqueness and not race.
Keywords: admixture, evolutionary lineage, gene flow, genetic differentiation, race, human evolution
1. The Biological Meaning of ‘Race’
Many human societies classify people into racial categories. These categories often have very real effects politically, socially, and economically. Even if race is culturally real, that does not mean that these societal racial categories are biologically meaningful. For example, individuals who classify themselves as “white” in Brazil are often considered “black” in the U.S.A., and many other countries use similar or identical racial terms in highly inconsistent fashions (Fish, 2002). This inconsistency is only reinforced when examined genetically. For example, Lao et al. (2010) assessed the geographical ancestry of self-declared “whites” and “blacks” in the United States by the use of a panel of geographically informative genetic markers. It is well known that the frequencies of alleles vary over geographical space in humans. Although the differences in allele frequencies are generally very modest for any one gene, it is possible with modern DNA technology to infer the geographical ancestry of individuals by scoring large numbers of genes. Using such geographically informative markers, self-identified “whites” from the United States are primarily of European ancestry, whereas U.S. “blacks” are primarily of African ancestry, with little overlap in the amount of African ancestry between self-classified U.S. “whites” and “blacks”. In contrast, Santos et al. (2009) did a similar genetic assessment of Brazilians who self-identified themselves as “whites”, “browns”, and “blacks” and found extensive overlap in the amount of African ancestry among all these “races”. Indeed, many Brazilian “whites” have more African ancestry than some U.S. “blacks”. Obviously, the culturally defined racial categories of “white” and “black” do not have the same genetic meanings in the United States and Brazil. The inconsistencies in the meaning of “race” across cultures and with genetic ancestry provide a compelling reason for a biological-based, culture-free definition of race. Another reason is that humans are the product of the same evolutionary processes that have led to all the other species on this planet. The subdivision of a species into groups or categories is not unique to our species. Since evolutionary biology deals with all life on this planet, biologists need a definition of race that is applicable to all species. A definition of “race” that is specific to one human culture at one point of time in its cultural history is inadequate for this purpose. Therefore, a universal, culture-free definition of race is required before the issue of the existence of races in humans (or any other species) can be addressed in a biological context.
The word “race” is not commonly used in the non-human biological literature. Evolutionary biologists have many words for subdivisions within a species (Templeton, 2006). At the lowest level are demes, local breeding populations. Demes have no connotation of being a major subdivision or type within a species. In human population genetics, even small ethnic groups or tribes are frequently subdivided into multiple demes, whereas “race” always refers to a much larger grouping. Another type of subdivision is “ecotype”, which refers to a group of individuals sharing one or more adaptations to a specific environment. Sometimes the defining environmental variable is widespread, so an ecotype can refer to a large geographical population. However, sometimes the environmental heterogeneity can exist on a small geographical scale. In such circumstances, a single local area with no significant genetic subdivision for almost all genes can contain more than one ecotype (e.g., Oberle & Schaal, 2011). Ecotypes are therefore not universally a major subdivision or type within a species, but sometimes merely a local polymorphism. Ecotypes cannot define “race” in a manner applicable to all species, and whether or not ecotypes can define human races will be addressed later. Of all the words used to describe subdivisions or subtypes within a species, the one that has been explicitly defined to indicate major geographical “races” or subdivisions is “subspecies” (Futuyma, 1986, pg. 107–109; Mayr, 1982, pg. 289). Because of this well-established usage in the evolutionary literature, “race” and “subspecies” will be regarded as synonyms from a biological perspective. In this manner, human “race” can be placed into a broader evolutionary context that is no longer species-specific or culturally dependent.
The question of the existence of human “races” now becomes the question of the existence of human subspecies. This question can be addressed in an objective manner using universal criteria. The Endangered Species Act of the USA mandates the protection of endangered vertebrate subspecies (Pennock & Dimmick, 1997). Accordingly, conservation biologists have developed operational definitions of race or subspecies that are applicable to all vertebrates, and two have been used extensively in the non-human literature. These two biological definitions of subspecies or “race” will be applied to humans and to our nearest evolutionary relative, the chimpanzee, in order to avoid an anthropocentric, culture-specific definition of race.
One definition regards races as geographically circumscribed populations within a species that have sharp boundaries that separate them from the remainder of the species (Smith, Chiszar, & Montanucci, 1997). In traditional taxonomic studies, the boundaries were defined by morphological differences, but now these boundaries are typically defined in terms of genetic differences that can be scored in an objective fashion in all species. Most demes or local populations within a species show some degree of genetic differentiation from other local populations, by having either some unique alleles or at least different frequencies of alleles. If every genetically distinguishable population were elevated to the status of race, then most species would have hundreds to tens of thousands of races, thereby making race nothing more than a synonym for a deme or local population. A race or subspecies requires a degree of genetic differentiation that is well above the level of genetic differences that exist among local populations. One commonly used threshold is that two populations with sharp boundaries are considered to be different races if 25% or more of the genetic variability that they collectively share is found as between population differences (Smith, et al., 1997). A common measure used to quantify the degree of differentiation is a statistic known as pairwise fst. The pairwise fst statistic in turn depends upon two measures of heterozygosity. The frequency with which two genes are different alleles given that they have been randomly drawn from the two populations pooled together is designated by Ht, the expected heterozygosity of the total population. Similarly, Hs is the average frequency with which two randomly drawn genes from the same subpopulation are different alleles. Then, fst=(Ht-Hs)/Ht. In many modern genetic studies, the degree of DNA sequence differences between the randomly drawn genes is quantified, often with the use of a model of mutation, instead of just determining if the two DNA sequences are the same or different. When this done, the analysis is called an Analysis of MOlecular VAriation (AMOVA), and various measures of population differentiation analogous to fst exist for different mutation models. Regardless of the specific measure, the degree of genetic differentiation can be quantified in an objective manner in any species. Hence, human races can indeed be studied with exactly the same criteria applied to non-human species. The main disadvantage of this definition is the arbitrariness of the threshold value of 25%, although it was chosen based on the observed amount of subdivision found within many species.
A second definition defines races as distinct evolutionary lineages within a species. An evolutionary lineage is a population of organisms characterized by a continuous line of descent such that the individuals in the population at any given time are connected by ancestor/descendent relationships. Because evolutionary lineages can often be nested together into a larger, more ancestral evolutionary lineage, the evolutionary lineages that are relevant for defining subspecies in conservation biology are the smallest population units that function as an evolutionary lineage within a species. The phylogenetic species concept elevates all evolutionary lineages to the status of species (Cracraft, 1989), but most species concepts allow for multiple lineages to exist within a species. For example, the cohesion species concept defines a species as an evolutionary lineage that maintains its cohesiveness over time because it is a reproductive community capable of exchanging gametes and/or an ecological community sharing a derived adaptation or adaptations needed for successful reproduction (Templeton, 1989, 2001). Two or more evolutionary lineages nested within an older lineage that are capable of exchanging gametes and/or share the same adaptations necessary for successful reproduction are considered lineages nested within a single cohesion species. The biological species concept only uses the criterion of gamete exchangeability and is a proper logical subset of the cohesion concept (Templeton, 1998b; Templeton, 2001). Hence, the biological species concept also allows multiple evolutionary lineages to exist within a species. The possibility of multiple evolutionary lineages within a species is commonly recognized in the area of conservation biology, and indeed the evolutionary lineage definition of race or subspecies has become the dominant definition in much of conservation and evolutionary biology, in large part because it is a natural historical population unit that emerges from modern phylogenetic theory and practice (Amato & Gatesy, 1994; Crandall, Binida-Emonds, Mace, & Wayne, 2000).
Many processes can create an evolutionary lineage. For example, hybridization can create a new lineage by either having the hybrid state stabilized (often through polyploidy) or having a stable recombinant type emerge (Templeton, 1981). This mode for the origin of new lineages is common in plants, but rare in vertebrates (Templeton, 1981). In terrestrial vertebrates, evolutionary lineages are commonly created within a species when an ancestral population is split into two or more subpopulations, often by some sort of geographical barrier, such that there is no or extremely limited genetic interchange after the split (Crandall, et al., 2000). Recall that lineages are defined in terms of ancestor/descendent relationships. DNA is the molecule that is passed on from ancestors to descendents, so genetic surveys provide a direct means of identifying lineages. The primary genetic impact of the establishment of a new evolutionary lineage is that the lineage accumulates genetic differences from the remaining descendents of the ancestral population with increasing time since the split. Immediately after the split, the subpopulations would share most ancestral polymorphisms (gene loci with more than one allele) and would therefore be difficult to diagnose as separate lineages. With increasing time since the split, genetic divergence accumulates and diagnosing the separate lineages becomes easier. A split into separate lineages also means that the genetic differences among the races would define an evolutionary tree analogous to an evolutionary tree of species. Statistical methods exist for testing the null hypothesis that the genetic variation within a species has a tree-like structure, and other statistics test the null hypothesis that the entire sample defines a single evolutionary lineage (Templeton, 1998b, 1999; Templeton, 2001). Therefore, just as with the fst definition, the lineage definition of race can be implemented in an objective fashion using uniform criteria, thereby avoiding an anthropocentric or cultural definition of race.
It is critical to note that genetic differentiation alone is insufficient to define a subspecies or race under either of these definitions of race. Both definitions require that genetic differentiation exists across sharp boundaries and not as gradual changes, with the boundaries reflecting the historical splits. These sharp boundaries are typically geographic, but not always. For example, even non-genetic behavioral differences, such as learned song dialects in birds or linguistic boundaries in humans, can serve as the basis for a sharp genetic boundary when these non-genetic traits are associated with evolutionary history. The fst definition in addition requires that the genetic differentiation across the geographical boundary exceeds a quantitative threshold, and the evolutionary lineage definition requires that the genetic differentiation fits a tree-like evolutionary structure. Hence, genetic differentiation is necessary but not sufficient to infer a race. Human populations certainly show genetic differences across geographical space, but this does not necessarily mean that races exist in humans.
Alan R. Templeton
Abstract
Races may exist in humans in a cultural sense, but biological concepts of race are needed to access their reality in a non-species-specific manner and to see if cultural categories correspond to biological categories within humans. Modern biological concepts of race can be implemented objectively with molecular genetic data through hypothesis-testing. Genetic data sets are used to see if biological races exist in humans and in our closest evolutionary relative, the chimpanzee. Using the two most commonly used biological concepts of race, chimpanzees are indeed subdivided into races but humans are not. Adaptive traits, such as skin color, have frequently been used to define races in humans, but such adaptive traits reflect the underlying environmental factor to which they are adaptive and not overall genetic differentiation, and different adaptive traits define discordant groups. There are no objective criteria for choosing one adaptive trait over another to define race. As a consequence, adaptive traits do not define races in humans. Much of the recent scientific literature on human evolution portrays human populations as separate branches on an evolutionary tree. A tree-like structure among humans has been falsified whenever tested, so this practice is scientifically indefensible. It is also socially irresponsible as these pictorial representations of human evolution have more impact on the general public than nuanced phrases in the text of a scientific paper. Humans have much genetic diversity, but the vast majority of this diversity reflects individual uniqueness and not race.
Keywords: admixture, evolutionary lineage, gene flow, genetic differentiation, race, human evolution
1. The Biological Meaning of ‘Race’
Many human societies classify people into racial categories. These categories often have very real effects politically, socially, and economically. Even if race is culturally real, that does not mean that these societal racial categories are biologically meaningful. For example, individuals who classify themselves as “white” in Brazil are often considered “black” in the U.S.A., and many other countries use similar or identical racial terms in highly inconsistent fashions (Fish, 2002). This inconsistency is only reinforced when examined genetically. For example, Lao et al. (2010) assessed the geographical ancestry of self-declared “whites” and “blacks” in the United States by the use of a panel of geographically informative genetic markers. It is well known that the frequencies of alleles vary over geographical space in humans. Although the differences in allele frequencies are generally very modest for any one gene, it is possible with modern DNA technology to infer the geographical ancestry of individuals by scoring large numbers of genes. Using such geographically informative markers, self-identified “whites” from the United States are primarily of European ancestry, whereas U.S. “blacks” are primarily of African ancestry, with little overlap in the amount of African ancestry between self-classified U.S. “whites” and “blacks”. In contrast, Santos et al. (2009) did a similar genetic assessment of Brazilians who self-identified themselves as “whites”, “browns”, and “blacks” and found extensive overlap in the amount of African ancestry among all these “races”. Indeed, many Brazilian “whites” have more African ancestry than some U.S. “blacks”. Obviously, the culturally defined racial categories of “white” and “black” do not have the same genetic meanings in the United States and Brazil. The inconsistencies in the meaning of “race” across cultures and with genetic ancestry provide a compelling reason for a biological-based, culture-free definition of race. Another reason is that humans are the product of the same evolutionary processes that have led to all the other species on this planet. The subdivision of a species into groups or categories is not unique to our species. Since evolutionary biology deals with all life on this planet, biologists need a definition of race that is applicable to all species. A definition of “race” that is specific to one human culture at one point of time in its cultural history is inadequate for this purpose. Therefore, a universal, culture-free definition of race is required before the issue of the existence of races in humans (or any other species) can be addressed in a biological context.
The word “race” is not commonly used in the non-human biological literature. Evolutionary biologists have many words for subdivisions within a species (Templeton, 2006). At the lowest level are demes, local breeding populations. Demes have no connotation of being a major subdivision or type within a species. In human population genetics, even small ethnic groups or tribes are frequently subdivided into multiple demes, whereas “race” always refers to a much larger grouping. Another type of subdivision is “ecotype”, which refers to a group of individuals sharing one or more adaptations to a specific environment. Sometimes the defining environmental variable is widespread, so an ecotype can refer to a large geographical population. However, sometimes the environmental heterogeneity can exist on a small geographical scale. In such circumstances, a single local area with no significant genetic subdivision for almost all genes can contain more than one ecotype (e.g., Oberle & Schaal, 2011). Ecotypes are therefore not universally a major subdivision or type within a species, but sometimes merely a local polymorphism. Ecotypes cannot define “race” in a manner applicable to all species, and whether or not ecotypes can define human races will be addressed later. Of all the words used to describe subdivisions or subtypes within a species, the one that has been explicitly defined to indicate major geographical “races” or subdivisions is “subspecies” (Futuyma, 1986, pg. 107–109; Mayr, 1982, pg. 289). Because of this well-established usage in the evolutionary literature, “race” and “subspecies” will be regarded as synonyms from a biological perspective. In this manner, human “race” can be placed into a broader evolutionary context that is no longer species-specific or culturally dependent.
The question of the existence of human “races” now becomes the question of the existence of human subspecies. This question can be addressed in an objective manner using universal criteria. The Endangered Species Act of the USA mandates the protection of endangered vertebrate subspecies (Pennock & Dimmick, 1997). Accordingly, conservation biologists have developed operational definitions of race or subspecies that are applicable to all vertebrates, and two have been used extensively in the non-human literature. These two biological definitions of subspecies or “race” will be applied to humans and to our nearest evolutionary relative, the chimpanzee, in order to avoid an anthropocentric, culture-specific definition of race.
One definition regards races as geographically circumscribed populations within a species that have sharp boundaries that separate them from the remainder of the species (Smith, Chiszar, & Montanucci, 1997). In traditional taxonomic studies, the boundaries were defined by morphological differences, but now these boundaries are typically defined in terms of genetic differences that can be scored in an objective fashion in all species. Most demes or local populations within a species show some degree of genetic differentiation from other local populations, by having either some unique alleles or at least different frequencies of alleles. If every genetically distinguishable population were elevated to the status of race, then most species would have hundreds to tens of thousands of races, thereby making race nothing more than a synonym for a deme or local population. A race or subspecies requires a degree of genetic differentiation that is well above the level of genetic differences that exist among local populations. One commonly used threshold is that two populations with sharp boundaries are considered to be different races if 25% or more of the genetic variability that they collectively share is found as between population differences (Smith, et al., 1997). A common measure used to quantify the degree of differentiation is a statistic known as pairwise fst. The pairwise fst statistic in turn depends upon two measures of heterozygosity. The frequency with which two genes are different alleles given that they have been randomly drawn from the two populations pooled together is designated by Ht, the expected heterozygosity of the total population. Similarly, Hs is the average frequency with which two randomly drawn genes from the same subpopulation are different alleles. Then, fst=(Ht-Hs)/Ht. In many modern genetic studies, the degree of DNA sequence differences between the randomly drawn genes is quantified, often with the use of a model of mutation, instead of just determining if the two DNA sequences are the same or different. When this done, the analysis is called an Analysis of MOlecular VAriation (AMOVA), and various measures of population differentiation analogous to fst exist for different mutation models. Regardless of the specific measure, the degree of genetic differentiation can be quantified in an objective manner in any species. Hence, human races can indeed be studied with exactly the same criteria applied to non-human species. The main disadvantage of this definition is the arbitrariness of the threshold value of 25%, although it was chosen based on the observed amount of subdivision found within many species.
A second definition defines races as distinct evolutionary lineages within a species. An evolutionary lineage is a population of organisms characterized by a continuous line of descent such that the individuals in the population at any given time are connected by ancestor/descendent relationships. Because evolutionary lineages can often be nested together into a larger, more ancestral evolutionary lineage, the evolutionary lineages that are relevant for defining subspecies in conservation biology are the smallest population units that function as an evolutionary lineage within a species. The phylogenetic species concept elevates all evolutionary lineages to the status of species (Cracraft, 1989), but most species concepts allow for multiple lineages to exist within a species. For example, the cohesion species concept defines a species as an evolutionary lineage that maintains its cohesiveness over time because it is a reproductive community capable of exchanging gametes and/or an ecological community sharing a derived adaptation or adaptations needed for successful reproduction (Templeton, 1989, 2001). Two or more evolutionary lineages nested within an older lineage that are capable of exchanging gametes and/or share the same adaptations necessary for successful reproduction are considered lineages nested within a single cohesion species. The biological species concept only uses the criterion of gamete exchangeability and is a proper logical subset of the cohesion concept (Templeton, 1998b; Templeton, 2001). Hence, the biological species concept also allows multiple evolutionary lineages to exist within a species. The possibility of multiple evolutionary lineages within a species is commonly recognized in the area of conservation biology, and indeed the evolutionary lineage definition of race or subspecies has become the dominant definition in much of conservation and evolutionary biology, in large part because it is a natural historical population unit that emerges from modern phylogenetic theory and practice (Amato & Gatesy, 1994; Crandall, Binida-Emonds, Mace, & Wayne, 2000).
Many processes can create an evolutionary lineage. For example, hybridization can create a new lineage by either having the hybrid state stabilized (often through polyploidy) or having a stable recombinant type emerge (Templeton, 1981). This mode for the origin of new lineages is common in plants, but rare in vertebrates (Templeton, 1981). In terrestrial vertebrates, evolutionary lineages are commonly created within a species when an ancestral population is split into two or more subpopulations, often by some sort of geographical barrier, such that there is no or extremely limited genetic interchange after the split (Crandall, et al., 2000). Recall that lineages are defined in terms of ancestor/descendent relationships. DNA is the molecule that is passed on from ancestors to descendents, so genetic surveys provide a direct means of identifying lineages. The primary genetic impact of the establishment of a new evolutionary lineage is that the lineage accumulates genetic differences from the remaining descendents of the ancestral population with increasing time since the split. Immediately after the split, the subpopulations would share most ancestral polymorphisms (gene loci with more than one allele) and would therefore be difficult to diagnose as separate lineages. With increasing time since the split, genetic divergence accumulates and diagnosing the separate lineages becomes easier. A split into separate lineages also means that the genetic differences among the races would define an evolutionary tree analogous to an evolutionary tree of species. Statistical methods exist for testing the null hypothesis that the genetic variation within a species has a tree-like structure, and other statistics test the null hypothesis that the entire sample defines a single evolutionary lineage (Templeton, 1998b, 1999; Templeton, 2001). Therefore, just as with the fst definition, the lineage definition of race can be implemented in an objective fashion using uniform criteria, thereby avoiding an anthropocentric or cultural definition of race.
It is critical to note that genetic differentiation alone is insufficient to define a subspecies or race under either of these definitions of race. Both definitions require that genetic differentiation exists across sharp boundaries and not as gradual changes, with the boundaries reflecting the historical splits. These sharp boundaries are typically geographic, but not always. For example, even non-genetic behavioral differences, such as learned song dialects in birds or linguistic boundaries in humans, can serve as the basis for a sharp genetic boundary when these non-genetic traits are associated with evolutionary history. The fst definition in addition requires that the genetic differentiation across the geographical boundary exceeds a quantitative threshold, and the evolutionary lineage definition requires that the genetic differentiation fits a tree-like evolutionary structure. Hence, genetic differentiation is necessary but not sufficient to infer a race. Human populations certainly show genetic differences across geographical space, but this does not necessarily mean that races exist in humans.