A Reduction of "Species" Resolves the Species Problem ------ Jody Hey, January 1997
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GENETIC DRIFT AND POPULATION STRUCTURE
For a group of organisms to be a genetic species, genetic drift must be creating a kind of
individual, meaning an entity with boundaries in space and time (Hull, 1976). Perhaps the clearest
example of a genetic species would be a group of organisms that are completely panmictic (i.e.
random mating) amongst themselves without the occurrence of any mating with organisms outside the
group. For asexual organisms, the criteria of completely random mating is replaced by one of
complete demographic exchangeability (Templeton, 1989). In an asexual group of organisms with
complete demographic exchangeability, any one organism's physical place and environmental role
could be taken by any other organism. However, complete panmixia or demographic exchangeability
need not be present in order for there to be a sharp boundary to the pattern of genetic drift. In
general, any time that a group of organisms occurs with gene flow or demographic exchangeability among the organisms, and where the level of gene flow or demographic exchangeability is high
relative to the level with organisms outside of the group, a boundary will exist (Templeton, 1989).
It is also possible for there to be variation in the degree to which organisms share genetic drift,
and this variation may not occur with sharp boundaries. Consider the case of isolation by distance
(Wright, 1943) in which the times of possible coancestry for a given pair of DNAs are proportional to
the physical distance between the members of that pair. Under this scenario the pattern of genetic
drift, as well as the pattern of genetic variation, among organisms may not be structured but may
follow a continuous pattern over some environmental landscape. A sample of DNAs will still have a
gene tree history, but the spacing of the nodes may vary widely and is expected to have a variance
larger than expected under a simple demographic model of shared genetic drift (Slatkin, 1987; Hey,
1991).
Another kind of population structure may lead to nested levels of demographic exchangeability
or gene flow, with multiple nested boundaries to the pattern of genetic drift. An example is the
population structure of Escherichia coli. Genetic drift may occur over a short time scale among the
cells in a single colony on a petri dish, and over a longer time scale among the population of cells
within the intestine of a single mammal. On a larger scale, exchange of E. coli cells occurs between
different individual intestinal populations, and this leads to turnover of individual intestinal populations
(Hartl and Dykhuizen, 1984). Thus the structure of E. coli
populations seems to include a hierarchy of levels of genetic drift.
Individuality, by the criterion of a boundary in the pattern of genetic drift,
occurs at multiple nested levels.
Another pattern not clearly consistent with shared genetic drift can arise when two sexual
populations share genetic drift for just a portion of the genome. They may share drift over the entire
genome with the exception of a single region that is under natural selection, with different functional
forms of the region maintained in different populations. Similarly, genetic drift may be shared for
organelle genomes but not nuclear genomes. At the other extreme are two populations that share drift
over very little of the genome because of natural selection. It is possible that these populations may
still generate hybrids with some reproductive success and share drift at parts of the genome that are
not linked to those that are under differential natural selection.
These scenarios of population structure and hybridization illuminate an area of uncertainty for
the biological species concept (Mayr, 1963, ch. 2). This can be seen by considering the very close
parallel between Dobzhansky's (1950) concept of a Mendelian population, and the genetic species
concept. Dobzhansky defined the smallest Mendelian population as a panmictic unit, and envisioned
larger Mendelian populations to be groups of panmictic units that engaged in gene flow. Finally, the
largest Mendelian populations are biological species. Dobzhansky envisioned the existence of a
boundary, a partition in the magnitude of gene flow such that there was a point when species could be
defined. However, the concept of a Mendelian population does not by itself imply the existence of
such a boundary. Dobzhansky's portrayal of nested levels of gene flow, beginning with high gene
flow and panmixia at the lower limit, does not necessarily imply the existence of a sharp boundary at
the upper limit where gene flow approaches zero. Under the biological species concept, the existence
of a sharp boundary to gene flow is attributed to the presence of isolating mechanisms that prevent
gene flow. The genetic species concept differs from the biological species concept in not having a
necessary role for any process other than genetic drift.
A focus on genetic drift as the essence of species provides a form of negative answer to some
aspects of the "species problem". All three of the situations described (complex population structure,
isolation by distance, and sexual populations with some genomic partitioning of gene flow) are
"problem cases" for which biologists are often at a loss for clear ways to delineate species. A
positive resolution of these uncertainties would be, for example, some description of the meaning of
"species" that permitted objective resolution of many problem cases. However, when these problem
cases are considered with the reduced concept of genetic species, the uncertainty of these situations
does not go away. In short, it appears that species are not a necessary consequence of those
processes that do often give rise to species. A similar negative resolution was also proposed by Leven
(1979) for many of the problem cases that occur among plants, especially those that rarely outcross or
have limited gamete dispersal and experience isolation by distance. In these cases, and others where
organsims do not occur in groups that share genetic drift, organisms do not occur as parts of species.
In the long term, it is expected that all organisms have histories that include periods when
ancestors were part of a genetic species. This is because the causes of genetic species, both mutational
and environmental, will sometimes create groups of organisms with periods of uniform genetic drift in
which the probability of recent coancestry for any pair of DNAs has little variation. A low variance
among pairs of DNAs for possible coancestry times is more likely for a group of DNAs among which
genetic drift is proceeding rapidly. Rapid genetic drift may result either from ecological circumstances
that sharply curtail reproduction or from the appearance of a strongly favored mutation. Also, with sex, rapid genetic drift can occur for a tightly linked portion of the genome as a result of advantageous
mutations or an abundance of deleterious mutations (Maynard Smith and Haigh, 1974; Kaplan et al.,
1989; Charlesworth et al., 1993). Thus environmental changes or mutations may create genetic species
from groups of organisms that are not in genetic species.
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© 1997 Jody Hey
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