26 Dec 2008, 5:25pm
Wildlife Management Wildlife Policy
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A Proposal to Eliminate Redundant Terminology for Intra-Species Groups

M. A. Cronin. 2006. A Proposal to Eliminate Redundant Terminology for Intra-Species Groups. Wildlife Society Bulletin 34(1):237–241; 2006

Dr. Matthew Cronin PhD. is Research Associate Professor of Animal Genetics, School of Natural Resources and Agricultural Sciences, University of Alaska Fairbanks. He is also a member of the Alaska Board of Forestry.

Full text [here]

Selected excerpts:


Many new terms have come into use for intra-species groups of animals defined with genetic criteria including subspecies, evolutionarily significant units, evolutionary units, management units, metapopulations, distinct population segments, populations, and subpopulations. These terms have redundant meanings and can lead to confusion for biologists, managers, and policy makers. I propose that for wildlife management we can simplify intra-species terminology and use only the terms subspecies, populations, and subpopulations. These 3 terms have roots in evolutionary and population biology and can incorporate genetic, demographic, and geographic considerations.

Recently, there has been a proliferation of terms used to describe groups of animals below the species level. For example, Wells and Richmond (1995) identified more than 30 terms used to describe groups generally referring to populations. They also discussed the problems with scientific communication associated with such extensive and redundant terminology.

The importance of intraspecies definitions is exemplified by the United States Endangered Species Act (ESA). The ESA allows listing of species, but it also allows listing of subspecies and distinct population segments (DPS) without clear definition of these terms. The importance of these intra-specific categories is evident in the large number of subspecies and DPS listed under the ESA. For example, more than 70% (57 of 81 listed taxa) of the listed mammals in the United States are identified as subspecies or DPS (http://endangered.fws.gov/wildlife.html). Examples of subspecies listed under the ESA with questionable subspecies status include the California gnatcatcher (Polioptila californica californica, Cronin 1997, Zink et al. 2000) and Preble’s meadow jumping mouse (Zapus hudsonius preblei, Ramey et al. 2005). Other examples of indefinite subspecies designations that affect management and policy are given by Cronin (1993) and Zink (2004).

The importance of clear definition of DPS has been recognized by the agencies administering the ESA (i.e., The United States Fish and Wildlife Service and National Marine Fisheries Service). These agencies noted: “Federal agencies charged with carrying out the provisions of the ESA have struggled for over a decade to develop a consistent approach for interpreting the term ‘distinct population segment’” (Waples 1991:v); and “…it is important that the term ‘distinct population segment’ beinterpreted in a clear and consistent fashion.” (Federal Register 7 Feb. 1996, Vol 61:4722). The National Research Council (NRC 1995:55) recognized the importance of identification of intraspecific units for ESA consideration and stated: “Unless we agree to preserve all endangered or threatened organisms of all taxonomic ranks, we must find ways to identify those groups of organisms we consider to be significant.

Genetics is increasingly being used to designate intra-specific groups, including subspecies, DPS, evolutionarily significant units (ESU), evolutionary units (EU), management units (MU), metapopulations, populations, and subpopulations (Moritz 1994, Moritz et al. 1995, NRC 1995, Avise 2000). These groups are partially or entirely defined by genetic similarity, often inferred from molecular genetic data. Genetic similarity is assumed to reflect recent common ancestry of, or extant gene flow among, groups of animals. Groups thus identified are frequently designated as a unit for management or conservation. In a previous paper, I discussed the utility and limitations of genetic data in wildlife management, including identification of units for management and conservation (Cronin 1993). I thought it would be useful to revisit this issue because of the introduction of new terms defined with genetic considerations. My objective in this paper is to review several intra-species terms defined with genetics (subspecies, ESU, EU, MU, metapopulation, DPS, population, subpopulation) and propose a way to simplify their use.

Intra-Species Groups

Before discussing intra-species groups, it is useful to define a species. The most common species concept is that of biological species, identified with a Latin binomial name (e.g., Odocoileus virginianus, white-tailed deer). Biological species are groups of interbreeding natural populations that are reproductively isolated from other such groups (Mayr 1963). Other species concepts are potentially useful (e.g., phylogenetic species, genetic species, Avise 1994, 2000, NRC 1995, Baker et al. 2003), but they are beyond the scope of this discussion. Identification of species with any of these concepts is not always definitive because of uncertainties about reproductive compatibility in natural populations, morphologically similar sibling species, and unknown phylogenetic relationships. However for most wildlife management applications, identification of species is not a problem compared to identification of intra-species groups. …


A subspecies has been defined as a geographically defined group of local populations which differ from other such groups (Mayr 1969, Dobzhansky 1970). Subspecies are given a Latin trinomial name in taxonomic classification (e.g., Odocoileus hemionus hemionus, Rocky Mountain mule deer; O. h. sitkensis, Sitka black-tailed deer). However, the subspecies concept has been criticized by several authors (Wilson and Brown 1953, Ryder 1986, Cronin 1997, Ehrlich 2000, Zink 2004). Wilson and Brown (1953) contended that the subspecies concept is so arbitrary a concept that it should be abandoned. Vanzolini (1992:189) noted that “…present applications of the subspecies concept are uneven, frequently undocumented, and lead to no improvement of either evolutionary theory or practical taxonomy.” Futuyma (1986) noted that there is so much variation among populations of most species that some combination of characters will distinguish each population from others and, consequently, there is no clear limit to the number of subspecies that can be recognized. Ehrlich (2000:49) echoed this sentiment: “Widespread species thus can be divided into any number of different sets of ’subspecies’ simply by selecting different characteristics on which to base them,” and he summarized the issue: “As is the case with other species, geographic variation in human beings does not allow Homo sapiens to be divided into natural evolutionary units. That basic point… has subsequently been demonstrated in a variety of organisms… and use of the subspecies (or race) concept has essentially disappeared from the mainstream evolutionary literature”
(Ehrlich 2000:291). …

Evolutionarily Significant Units and Evolutionary Units

The term Evolutionarily Significant Unit (ESU) originally was suggested by zoo biologists as a potential substitute for the subspecies category in conservation efforts (Ryder 1986). However, the concept has taken on 2 definitions in the literature and relies on somewhat arbitrary criteria (Avise 2000, Milius 2000, DeWeerdt et al. 2002).

One definition of an ESU is a group with monophyletic mitochondrial DNA (mtDNA) and significant allele frequency differences at nuclear loci compared to other groups (Moritz 1994, Moritz et al. 1995). Other authors also recommend the use of a phylogenetic approach for identification of ESUs (Bernatchez 1995, Mayden and Wood 1995). Evolutionarily Significant Units defined by monophyletic mtDNA essentially conform to the recent subspecies definition as described above (Avise and Ball 1990). MtDNA phylogeny is described elsewhere (e.g., Cronin 1993; Avise 1994, 2000), but basically it refers to the genealogical relationships of mtDNA genotypes as inferred from DNA sequence analysis. Genotypes with similar DNA sequences are considered as sharing a more recent common ancestral genotype than divergent genotypes. It is important to recognize that this approach has potential flaws because mtDNA phylogeny (which represents a single gene phylogeny) may not reflect the overall differentiation of species or populations (Pamillo and Nei 1988, Cronin 1993).

A second definition of ESU has been applied to Pacific salmon and steelhead (Oncoryhnchus spp.) by the National Marine Fisheries Service (NMFS). In this case an ESU is a population (or a group of populations) that is substantially reproductively isolated from con-specific population units, and represents an important component in the evolutionary legacy of the species (Waples 1991, 1995). Such ESUs are considered distinct population segments (DPS) under the ESA. Substantial reproductive isolation refers to limited gene flow between ESUs, often measured with molecular genetic markers. … This definition of ESU differs from that of Moritz (1994) and Moritz et al. (1995) primarily because substantial reproductive isolation, not mtDNA phylogeny, is used to differentiate groups.

There are obvious problems with the NMFS definition of ESU. First, note in the definition that an ESU is a population or group of populations, so it is a redundant term. Second, the term has an inherent value judgment (evolutionary significance) and reliance on arbitrary criteria. Neither the degree of reproductive isolation (substantial) nor the evolutionary significance (importance to the evolutionary legacy of the species) of populations is quantitatively defined. The indefinite nature of the term “evolutionarily significant” is one of the reasons why the National Research Council coined the term Evolutionary Unit (EU), without the word “significant” (NRC 1995). Third, ESU appears to be an exclusive term, and some populations will warrant this status; some will not. However, in the case of Pacific salmonids (chinook salmon Oncorhynchus tshawytscha, Myers et al. 1998; coho salmon O. kisutch, Weitkamp et al. 1995; steelhead, anadromous O. mykiss, Busby et al. 1996), all wild fish are in one ESU or another. Except for hatchery fish, there are no nonevolutionarily significant units. One could ask, if every group is evolutionarily significant, then why have the term? The term ESU was instituted to avoid the subjective and arbitrary designations of many subspecies (Ryder 1986), but has itself become subjective and arbitrary.

Populations, Subpopulations, Distinct Population Segments, and Metapopulations

Population is perhaps the most general and widely used term for intra-species groups (Wells and Richmond 1995), and entire fields of study employ this term (e.g., population biology, population genetics). Populations of fish, marine mammals, and other aquatic animals often are referred to as stocks and the reader may consider this term synonymous with population for this discussion. At the highest level, the entire species can be considered an inclusive population (Dobzhansky 1970). At the middle level, a population can be considered as a group of component local populations or subpopulations. At the lowest level, a population is a group of individuals of a species in one geographic location (Mayr 1963). The terms deme, subpopulation, or local population are synonymous with this meaning. …

Another term with considerable importance in wildlife management is distinct population segment (DPS), which are units that can be listed under the ESA. As noted above, the NMFS designation of ESU is equivalent to a DPS for Pacific salmon and steelhead. Other groups, including fish, birds, and mammals, have been designated DPS for ESA purposes (http://endangered.fws.gov/wildlife.html). The criteria for designating a DPS include “…discreteness of the population segment in relation to the remainder of the species to which it belongs.” (Federal Register 7 Feb. 1996, Vol 61:4725). A population may be considered discrete if it is “markedly separated from other populations of the same taxon as a consequence of physical, physiological, ecological, or behavioral factors. Quantitative measures of genetic or morphological discontinuity may provide evidence of this separation.”
(Federal Register 7 Feb. 1996, Vol 61 4725). …

Management Units

The term management unit (MU) has recently been defined with genetic criteria. An MU is a demographically independent population or set of populations identified by differences in frequencies of mtDNA haplotypes or nuclear alleles, regardless of allele phylogeny (Moritz 1994; Moritz et al. 1995). Basically, an MU is a group with limited gene flow with other groups. In this genetic context, an MU can be considered synonymous with a subpopulation, local population, or DPS. Of course, the term management unit can be used in a completely nongenetic context, and management units frequently are based simply on geography, demography, or other factors (Cronin 1993, 1997, 2003, Avise 1995, Taylor and Dizon 1996).

A Proposal to Simplify Terms for Intra-Species Groups

It is clear from the preceding discussion and previous work (Wells and Richmond 1995), that the use of intra-species terms is inconsistent, redundant, and confusing. The terms ESU, EU, MU, and metapopulation resulted largely from genetics considerations (Waples 1991, 1995, Moritz 1994, Moritz et al. 1995, Hanski and Simberloff 1997). The term DPS resulted from a regulatory phrase (Federal Register 7 Feb. 1996, 61 FR 4722). The terms subspecies, population, and subpopulation are from pioneering research, thought, and syntheses on variation in natural populations (Mayr 1963, 1969; Dobzhansky 1970, Wright 1978).

In summary, aside from details that are largely irrelevant to wildlife management, it is reasonable to conclude that:

Subspecies = ESU (Mortiz 1994, definition) or EU;

Population = ESU (NMFS definition), subpopulation, EU, MU, or DPS;

Subpopulation = local population, deme, ESU (NMFS definition), EU, MU, or DPS.

Population composed of subpopulations = metapopulation composed of populations.

I propose that this redundancy can be eliminated if we restrict our use of intra-species terms to subspecies, population, and subpopulation. I would defer to those working with fish, marine mammals, and other aquatic animals if they prefer the terms stock and substock in lieu of population and subpopulation. The terms ESU, EU, MU, DPS, and metapopulation are not necessary for wildlife management. …

My proposal is not intended to ignore the contribution of genetics to wildlife management, but to simplify the use of terms. The use of the terms subspecies, population, and subpopulation
allow consideration of genetics, in addition to demography and geography. …

Ironically, the proliferation of terms created to describe intraspecific variation mimics the pre-evolutionary “typological thinking” in which variable groups (e.g., species, subspecies) were sorted into rigid classes. Darwin and the evolutionary synthesis of the 1900s instituted “population thinking,” in which it is recognized that organisms occur in variable populations, not constant types (Mayr 2001). Now we have developed a confusing array of classes (i.e. terms) to describe what are basically populations. I see nothing to be gained from forcing groups of animals into an increasing array of redundant classes. I believe that use of simple terms, with appropriate descriptions of the variation within and between them, is the best way to maintain population thinking in the application of science in wildlife management.

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