A Role for Molecular Genetics in the Recognition and Conservation of Endangered Species

Taxonomies based on morphological traits alone sometimes provide inadequate or misleading guides to phylogenetic distinctions at the subspecies and species levels. Yet taxonomic assignments inevitably shape perceptions of biotic diversity, including recognition of endangered species. Case histories are discussed in which the data of molecular genetics revealed prior systematic errors of the two possible kinds: taxonomic recognition of groups showing little evolutionary differentiation, and lack of taxonomic recognition of phylogenetically distinct forms. In such cases, conservation efforts for 'endangered species' can be misdirected with respect to the goal of protecting biological diversity.


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ing management strategies based solely on maximizing intrapopulation genetic variation: there appears to be wide variation among species in the fitness cost of inbreedings; many species in nature have breeding systems (e.g. self fertilization or sib mating) or geographic population structures that reduce heterozygosity far below its expected value under outcrossing and high gene flow; and matings between dissimilar individuals, while increasing variation in progeny, may sometimes disrupt favorable gene combinations and result in 'outbreeding depression'6.
Nonetheless, attention to intrapopulation genetic variation is likely to continue, because heterozygosity (as estimated by various molecular genetic techniques) is known to be dramatically reduced in some threatened species7-'0, and because such reductions are sometimes associated with lowered components of fitnessll,lz.
However, the connections between heterozygosity and population viability are complex, and in this respect molecular genetic data cannot provide unambiguous guidelines for the management of rare species. Molecular genetic information can still be of considerable value in another context, involving the appraisal of phylogenetic discontinuities within and among 'species'. Taxonomic assignments at the subspecies and species level, many of which were proposed in the last century from small numbers of morphological characters, continue to provide the systematic framework within which endangered forms are recognized.
Yet these taxonomic assignments too often provide inadequate or even incorrect partitions of phylogenetic diversity. An updated taxonomy that includes input from molecular genetics should provide a firmer foundation for the proper recognition and hence management of biotic diversity.
As examples, I will briefly summarize two case histories involving NorthAmericanendangered'species' in which the existing taxonomies improperly summarized the evolutionary genetic relationships of the populations involved. Full details and background references can be found in Refs 13 and 14, respectively.

Taxonomy-based mismanagement of endangered species Colonial pocket gopher
In 1898, Geomys colonus was described as a distinct species, with range confined to Camden County, Georgia. This form remained essentially unnoticed and unstudied until the 196Os, when gophers in Camden County were 'rediscovered'. The population referable to 'co/onus' then consisted of less than 100 individuals, and was subsequently listed and managed as an endangered species by the State of Georgia.
Subsequently, a molecular genetic survey was conducted using multilocus protein electrophoresis, karyotypic examination, and restriction enzyme analysis of mitochondrial DNA (mtDNA). None of these genetic methods detected any consistent distinction between 'colonus' and nearby populations of a common congener G. pinetis. This result was not attributable to a lack of sensitivity of the techniques employed, because each method revealed dramatic genetic differences among a broader geographic array of G. pinetis populations. The conclusion in this case was clear: 'G. colonus' did not warrant recognition as a distinct species. Either the species description in 1898 was inappropriate, or an original valid G. colonus species had gone extinct and was replaced by recent G. pinetis immigrants into Camden County.

Dusky seaside sparrow
In 1872, a melanistic form of seaside sparrow was discovered and subsequently described as a distinct species, Ammodramus nigrescens. suites of characters. A tree constructed from a given gene or character can be different from a population phylogeny, particularly when the divergence time between taxa is short22,23. But as divergence times between taxa increase (relative to effective population size), so too do the expected numbers of independent character states that concordantly identify the clades as monophyletic.

Its range was confined to Brevard County, Florida, whereas other seaside sparrow populations (A. maritimus) occur in coastal marshes from
In addition, historical biogeographic information will contribute importantly to the recognition of phylogenetic separations, particularly when geographic and genetic subdivisions are concordant.

Conclusion
There are currently over 500 species listed in the United States as endangered or threatenedzd, with perhaps 1000 more awaiting formal assessment15. Clearly, because of the time and expense involved, not all such taxa can be evaluated extensively by molecular genetic methods, nor need they be. Many endangered species are indisputably unique, with no close living relatives; conversely, identification of morphologically cryptic species by molecular methods may not be a high priority in conservation biology books when protection efforts for known species are already inadequate. Given the problems of environmental deterioration and species extinction on a global scale, it might be unwise to divert a large fraction of the limited resources earmarked for conservation to molecular genetic evaluations.
Nonetheless, in certain situations molecular genetic assessments are clearly a necessary and important guide to the description of biotic diversity. Furthermore, general management implications may often stem from studies funded as 'pure' research in molecular evolution. For example, Bermingham and Avise found that populations within each of several species of freshwater fishes in the southeastern United States exhibit marked and geographically concordant genetic differences, probably due to historical patterns of drainage isolation and coalescence.
These phylogenetic subdivisions should aid in the development of a regional management program applicable to many fish species in the southeast of the country. Molecular genetic techniques should be increasingly employed as an aid to phylogeny reconstruction, and hence biotic diversity assessment. The need for increased attention to molecular descriptions of phylogenetic differences, particu-larly at the level of populations and species, is a special aspect of the broader call to revive the field of systematics in conservation biol-ogy26. Considerable conservation resources are devoted to the management of rare taxa; commensurate attention should be devoted to the adequacy of the biotic descriptions.