the Florida panther led to specific interven- POLICY FORUM ECOLOGY w tion to inampase genetic diiersity (7) Stud-

DNA Banks for Endangered Animal Species

ies of evolutionary systematics using DNA markers have provided new insights such as the origin of whales (8) and assist in identifying appropriate for conserva- tion in many taxa for example crocodilians (91 and the African cichlids (10)

Oliver A Ryder Anne Mclamn Sydney Brsnnerh-Ping Zhang Kurt Benirschke Black rhinos are declining h Africa at alarming rates there were about 65000

A lthough the loss of biodiversity re- the biodiversity they encompass hinders throughout Afiica in 1970 but there were sulting from extinctions is receiving current study may place inappropriate pres- only about 2600 in 1999 (11) As part of the increasing attention the accompany- sure on natural populations and leaves the effort to assess the problem extensive anal-

ing decrease in access to genetic resources present generation ignorant about a portion yses of mitochondrial DNA diversity and has not been widely discussed The threat of its legacy to the future nuclear microsatellite polymorphism are of extinction for many species both known Genetic resource collections now pro- currently being performed to distinguish be- and as yet undiscovered vide essential tools that facili- tween the Southern and Eastern black rhino grows ever greater as whole ampbates tate scientific study F O ~ exam- populations (12) Phylogeographic studies ecosystems vanish human Respond u ple the comparisons of in- are also continuing for the giant panda (13) populations proliferate and httpJlwwwsciencemag traspecific diversity between International Whaling Commission ef- human-mediated interference o~c-iconten~summaryl humans chimpanzees and go- forts to conserve cetaceans by regulating increases Even though efforts 2885464275 rillas are enriching our under- commercial and scientific whaling activi- to compile listings of threat- standing of human evolu- ties include prohibitions on taking ened plants and animals are developing (I) tion (3) Studies of mitochondria1 some species such as blue whales current views of timing of recovery from diversity have been used in coa-

A and all species of dolphins

anthropogenic extinctions suggest that lescent dating to determine the The ongoing monitoring of many millions of years will be required for evolutionary time back to a commercial products to replenishment to present-day levels (2) single ancestor for the chee- make sure that dolphin

The establishment and scientific man- tah (4) and for felids In be- meat and certain prohibit- agement of nature reserves and national havioral ecology scientists ed species of whales are parks in as many parts of the world as possi- interested in determining not included depends on ble is impemtive This is especially true for whether female sea turtles

) forensic DNA analyses

the tropics where the largest numbers of return to the same beaches which require reference threatened and endangered species may re- when nesting have relied DNA collections (14) side Major efforts to preserve biological di- on DNA restriction frag- I Captive breeding pro- versity are under way through habitat con- ment length polymor-

I vides an insurance policy

servation other in siru support living col- phisms (RFLPs) (5) and for some species may lections as maintained in botanical gardens In the foreseeable fu- w be the only hope of sur- arboreta and ~001ogical parks gamete and ture DNA sequencing will Genetic information is being vival It requires considera- seed banks f a species of agricultural inter- be fully automated and our used t o save tha California tion of small population est and the amassing and documentation of descendants will be able condor from extinction vulnerabilities to preserve museum specimens However relatively lit- rapidly to derive the se- high levels of genetic diver- tle effort has been made to collect and docu- quence of any organism whose DNA has sity In some instances input from reproduc- ment DNA specimens as genetic resources been appropriately collected and stockpiled tive physiologists to promote the establish- Yet the most fundamental derivative of a If genomes are available they will ment of pregnancies for example by artifl- species is the information in its genome be able not only to reconstruct what the or- cial insemhation contributes in a major way currently most easily preserved in the form ganism was like but also what its evolution- to the genetic preservation goals Cryo- of purified high-molecular-weight DNA ary relationships were how specific genes preservation of gametes and embryos has a Although the lack of emphasis on genetic arose to encode proteins that perform spe- role to play whereas in the future nuclear resource collections especially DNA banks cialized fimtions and how regulatory pro- replacement cloning h m established cell may be considered appropriate in the wn- gramming evolved The medical value of lines might prove of value If the cell lines text of current conservation priorities the such DNA banks should not be overlooked were made before numbers dropped danger- lack of howledge about their existence and and will undoubtedly provide materials that ously low the earlier level of genetic diversi-

m will contribute to advances in medicine and tv miht be restored (19 0A Ryder is the h t e r for Reproduction of Endan- gered Specie Zoological Society of San Diego CA 921124551 USA E-mail orydeampucsdedu A Mclaren

$ is at WellcomeKRC Institute Unlvwsity of Cambridge 8 CB2 1QR UK E-mail A McLarenwelccamacuk 5

Brenner is at the Mdecuhr Sciences Institute Berkaq

I CA 94704 USA E-mail sbrennermolsciorg Y-P Zhang is at the Key Laboratory of Cellular and Molecu- lar Evolution Kunming Institute of Zoology Chinese Academy of Sciences Kunming China E-mail zhangyppublIckmycn K Benirschke is at the De- partment of Pathology Univeaity of California San Diego CA 92093 USA E-mail kbenirscucsdedu

pharmaceutical development Determina- tion of ancestral character states for single nucleotide polymorphisms (SNPs) assists in interpreting the influence of selection on loci within the human genome (6)

Assessment of genetic resources can serve a valuable planning purpose in the overall conservation effort as well as in de- termination and management of the well- being of species and the richness of ecosys- tems Examination of genetic diversity of

- G o n e example of ongoing use of genet- ic information breeding efforts to save the California condor have been significantly aided by minisatellite RFLP variation from which kinship could be inferred (16) (see the figure) This is a species that had to be placed into captivity in order to save it from extinction (1 7) Risks of genetic diseases are important considerations in the management and survival of endangered species which typically have small population sizes (18) A

wwwsciencemagorg SCIENCE VOL 288 14APRIL 2000

S C I E N C E S C O M P A S S

heritable chondrodystrophy has been identi- fied in California condors (19)and its man- agement through identification of a linked marker to detect camers may be feasible in part because of banked DNA samples DNA banking has also been crucial for the preservation of Przewalskis wild horses through breeding programs that are attempt- ing to conserve a limited gene pool derived from 12 wild-caught individuals

Such strategies may succeed in saving a small fraction of endangered species at least for a time Resources for conserva- tion are limited and many species are found only in inaccessible places in im- poverished countries

The work of museums in botanical gar- dens and conservation of biological diver- sity through the collection identification cataloging of specimens an4 in some in- stances tissues is an underpinning effort However for many species of both verte- brate and invertebrate animals if nothing more is done our descendants will be left with little else than brief descriptions in scientific papers and voucher specimens in museums with only limited use for com- parative genomic studies

Although efforts are under way to es- tablish integrated databases we suggest that emphasis be placed on banking genet- ic resources even as the strategic cata- loging efforts are under way Currently a limited and relatively uncoordinated effort exists to preserve tissues gametes and frozen viable cells although some catalogs of genetic resource specimens are current- ly available online (20) A laudable effort is being made to organize seed banks for plants (21)

The technical aspects of saving DNA are straightforward Any tissue samples can be simply stored at -70degC or in liquid nitrogen DNA can be isolated from fresh or frozen tissue samples and purified DNA may be preserved for hundreds to thousands of years at room temperature provided it is kept dry for example in a closed vial of inert gas

We urge that a coordinated worldwide attempt be made to store for every endan- gered animal species samples of DNA DNA libraries or frozen cells or tissues that could readily yield DNA This might comprise under current estimates at least 5200 recognized species (22) There will of course be many difficult issues to ad- dress Access to endangered species con- sistent with their protection will require consideration by the signatories of the Convention on International Trade in En- dangered Species which has tended to im- pede transfer of specimens for biological research Intellectual property considera- tions and sovereignty issues under Article

15 of the Convention on Biological Diver- sity (23) sharing of rights to access and potential benefits need for duplicate col- lections and international coordination are controversial issues that need to be ad- dressed Strategies for organizing interna- tional coordination need to be developed We recognize that local communities and national governments have rights over their natural resources including genetic re- sources Conservation at every level must always involve local human populations

Our proposal is first to establish a means of collecting information on DNA banking efforts for endangered species of animals and second to encourage efforts to bank documented DNA specimens for the future Efforts in this direction are al- ready under way largely adjunct to partic- ular medical or agricultural research pro- jects For example collections of DNA are held at the Center for Reproduction of En- dangered Species of the San Diego Zoo the Laboratory of Genomic Diversity at the US National Cancer Institute and the Kunming Institute of Zoology from a vari- ety of mammals birds and freshwater fishes Collections of DNA from agricul- tural plants and animals are being assem- bled and distributed (24) and DNA speci- mens from botanical collections are also being made available (25)

Although it is difficult to estimate ac- curately costs for a global effort an annu- al cost per site for labor and materials in the United States for technical assistance supplies and freezers for unprocessed specimens might amount to $50000 to $80000 Benford (17 ) has estimated costs for saving examples for future analysis of species in rainforests by storage in liquid nitrogen at about $20 million per year DNA banks for recognized endangered species of animals would be less inclu- sive but would also be less costly and of more immediate practical value

To the best of our knowledge there have been no systematic attempts to coor- dinate or even to register these efforts let alone to extend them to endangered species worldwide We therefore propose to set up a Web-based method to register DNA banks Such a register should in- clude taxonomic information number of accessions geographic reference to collec- tion location andlor pedigree information (for example from a zoo studbook) and who is responsible for the collection This would reveal the extent of what exists al- ready and would help to structure the con- servation communitys thinking about the magnitude of the task

Participation in generating a listing of banked DNA specimens from endangered species of animals would not require mak-

ing samples available However as a first practical step a catalog of DNA specimens might build interest in creation of genomic libraries for a wide variety of studies We encourage suggestions about the design of the Web site for collecting information on DNA collections from endangered animal species and participation of the scientific and conservation communities in the un- dertaking of this effort Individuals and in- stitutions interested in receiving additional information including the announcement of the Web site for collecting information about DNA collections may contact DNA-bankssandiegozooorg

References and Notes 1 1996 International Conservation Union (IUCN) List of

Threatened Animals IUCN List of Threatened Plants Nat ional Biological lnformation Infrastructure (wwwnbiigov) (1997) H Saarenmaa The Global Biodiversity lnformation Facility Architectural and Implementation Issues (European Environmental Agency Tech Rep 34 Copenhagen 1999) 34 pp (wwweioneteuintgbifgbif-implementation-latesthtml)

2 JW Kirchner and AWeil Nature 404 177 (2000) 3 M Ruvolo Annu Rev Anthropol 26 515 (1997) P

Gagneux et dl Proc Natl Acad Sci USA 96 5077 (1999)

4 M Menotti-Raymond and S J OBrien Proc Natl Acad Sci USA 90 3172 (1993)

5 BW Bowen et dl Evolution48 1820 (1994) 6 1G Hacia etal Nature Genet 22 164 (1999) 7 PW Hedrick Conserv Biol 9 996 (1995) M E Roelke

JS Martenson S J OBrien Curr Biol 3 340 (1993) S1OBrien et dl Natl Geogr Res 6485 (1990)

8 M Shimamura et dl Nature 388666 (1997) 9 GAmato J Gatesy P Brazaitis in Molecular Evolution

Approaches and Applications R DeSalle and B Schier- water Eds (Birkhauser Basel Switzerland 1998) pp 177-189

10 W E Mayer HTichy J Klein Heredity80 702 (1998) 11 See wwwrhinos-irforg 12 M Jama R R Ramey 0Ryder M Houck RAman un-

published data 13 Y Zhang et dl Science China Ser C Life Sci 40210

(1997) 14 S R Palumbi and F Ciprianoj Hered 89 459 (1998)

C S Baker F Cipriano S R Palumbi Mol Ecol 5 671 (1996) F Cipriano and S R Palumbi Nature 397 307 (1999)

15 0A Ryder and K Benirschke Zoo Biol 16 295 (1997)

16 C J Geyer OA Ryder L G Chemnick EAThompson Mol Biol Evol 10571 (1 993)

17 G Benford Proc Natl Acad Sci USA 89 11098 (1 992)

18 OA Ryder Nature 331396 (1988) 19 K Ralls J D Ballou B A Rideout R Frankham Anim

Consen in press 20 RlKEN Gene Bank (wwwrtcrikengojp) American

Type Culture Collection (wwwatccorg) 21 Millennium Seed Bank (wrbgkeworgukseedbank

msbhtml) 22 List of Threatened Animals Wildlife Conservation and

Monitoring Centre (wwwwcmcorguk) 23 Convention on Biological Diversity (wbiodivorg

chmconvdefaulthtm) 24 Japanese Ministry of Agriculture Forestry and Fish-

eries (httpbankdnaaffrcgojp) 25 Missouri Botanical Garden St Louis MO USA

(wwwmobotorglMOBOTresearchDNAdocsl dnabankhtml)

26 This initiative is recognized as part of the Interna- tionalYear of the Biosphere (IBOY) an activity of DI- VERSITAS a creation of UNESCO and the Interna- tional Council of Scientific Unions (ICSU) and forms part of the effort to engender international coopera- tion in research and decision-making as a critical ele- ment for solving global environmental problems such as the accelerating loss of biodiversity We thank j Soberon R Medellin and an anonymous reviewer for helpful comments and suggestions

wwwsciencemagorg SCIENCE VOL 288 14APRIL 2000 277

S C I E N C E S C O M P A S S

heritable chondrodystrophy has been identi- fied in California condors (19)and its man- agement through identification of a linked marker to detect camers may be feasible in part because of banked DNA samples DNA banking has also been crucial for the preservation of Przewalskis wild horses through breeding programs that are attempt- ing to conserve a limited gene pool derived from 12 wild-caught individuals

Such strategies may succeed in saving a small fraction of endangered species at least for a time Resources for conserva- tion are limited and many species are found only in inaccessible places in im- poverished countries

The work of museums in botanical gar- dens and conservation of biological diver- sity through the collection identification cataloging of specimens an4 in some in- stances tissues is an underpinning effort However for many species of both verte- brate and invertebrate animals if nothing more is done our descendants will be left with little else than brief descriptions in scientific papers and voucher specimens in museums with only limited use for com- parative genomic studies

Although efforts are under way to es- tablish integrated databases we suggest that emphasis be placed on banking genet- ic resources even as the strategic cata- loging efforts are under way Currently a limited and relatively uncoordinated effort exists to preserve tissues gametes and frozen viable cells although some catalogs of genetic resource specimens are current- ly available online (20) A laudable effort is being made to organize seed banks for plants (21)

The technical aspects of saving DNA are straightforward Any tissue samples can be simply stored at -70degC or in liquid nitrogen DNA can be isolated from fresh or frozen tissue samples and purified DNA may be preserved for hundreds to thousands of years at room temperature provided it is kept dry for example in a closed vial of inert gas

We urge that a coordinated worldwide attempt be made to store for every endan- gered animal species samples of DNA DNA libraries or frozen cells or tissues that could readily yield DNA This might comprise under current estimates at least 5200 recognized species (22) There will of course be many difficult issues to ad- dress Access to endangered species con- sistent with their protection will require consideration by the signatories of the Convention on International Trade in En- dangered Species which has tended to im- pede transfer of specimens for biological research Intellectual property considera- tions and sovereignty issues under Article

15 of the Convention on Biological Diver- sity (23) sharing of rights to access and potential benefits need for duplicate col- lections and international coordination are controversial issues that need to be ad- dressed Strategies for organizing interna- tional coordination need to be developed We recognize that local communities and national governments have rights over their natural resources including genetic re- sources Conservation at every level must always involve local human populations

Our proposal is first to establish a means of collecting information on DNA banking efforts for endangered species of animals and second to encourage efforts to bank documented DNA specimens for the future Efforts in this direction are al- ready under way largely adjunct to partic- ular medical or agricultural research pro- jects For example collections of DNA are held at the Center for Reproduction of En- dangered Species of the San Diego Zoo the Laboratory of Genomic Diversity at the US National Cancer Institute and the Kunming Institute of Zoology from a vari- ety of mammals birds and freshwater fishes Collections of DNA from agricul- tural plants and animals are being assem- bled and distributed (24) and DNA speci- mens from botanical collections are also being made available (25)

Although it is difficult to estimate ac- curately costs for a global effort an annu- al cost per site for labor and materials in the United States for technical assistance supplies and freezers for unprocessed specimens might amount to $50000 to $80000 Benford (17 ) has estimated costs for saving examples for future analysis of species in rainforests by storage in liquid nitrogen at about $20 million per year DNA banks for recognized endangered species of animals would be less inclu- sive but would also be less costly and of more immediate practical value

To the best of our knowledge there have been no systematic attempts to coor- dinate or even to register these efforts let alone to extend them to endangered species worldwide We therefore propose to set up a Web-based method to register DNA banks Such a register should in- clude taxonomic information number of accessions geographic reference to collec- tion location andlor pedigree information (for example from a zoo studbook) and who is responsible for the collection This would reveal the extent of what exists al- ready and would help to structure the con- servation communitys thinking about the magnitude of the task

Participation in generating a listing of banked DNA specimens from endangered species of animals would not require mak-

ing samples available However as a first practical step a catalog of DNA specimens might build interest in creation of genomic libraries for a wide variety of studies We encourage suggestions about the design of the Web site for collecting information on DNA collections from endangered animal species and participation of the scientific and conservation communities in the un- dertaking of this effort Individuals and in- stitutions interested in receiving additional information including the announcement of the Web site for collecting information about DNA collections may contact DNA-bankssandiegozooorg

References and Notes 1 1996 International Conservation Union (IUCN) List of

Threatened Animals IUCN List of Threatened Plants Nat ional Biological lnformation Infrastructure (wwwnbiigov) (1997) H Saarenmaa The Global Biodiversity lnformation Facility Architectural and Implementation Issues (European Environmental Agency Tech Rep 34 Copenhagen 1999) 34 pp (wwweioneteuintgbifgbif-implementation-latesthtml)

2 JW Kirchner and AWeil Nature 404 177 (2000) 3 M Ruvolo Annu Rev Anthropol 26 515 (1997) P

Gagneux et dl Proc Natl Acad Sci USA 96 5077 (1999)

4 M Menotti-Raymond and S J OBrien Proc Natl Acad Sci USA 90 3172 (1993)

5 BW Bowen et dl Evolution48 1820 (1994) 6 1G Hacia etal Nature Genet 22 164 (1999) 7 PW Hedrick Conserv Biol 9 996 (1995) M E Roelke

JS Martenson S J OBrien Curr Biol 3 340 (1993) S1OBrien et dl Natl Geogr Res 6485 (1990)

8 M Shimamura et dl Nature 388666 (1997) 9 GAmato J Gatesy P Brazaitis in Molecular Evolution

Approaches and Applications R DeSalle and B Schier- water Eds (Birkhauser Basel Switzerland 1998) pp 177-189

10 W E Mayer HTichy J Klein Heredity80 702 (1998) 11 See wwwrhinos-irforg 12 M Jama R R Ramey 0Ryder M Houck RAman un-

published data 13 Y Zhang et dl Science China Ser C Life Sci 40210

(1997) 14 S R Palumbi and F Ciprianoj Hered 89 459 (1998)

C S Baker F Cipriano S R Palumbi Mol Ecol 5 671 (1996) F Cipriano and S R Palumbi Nature 397 307 (1999)

15 0A Ryder and K Benirschke Zoo Biol 16 295 (1997)

16 C J Geyer OA Ryder L G Chemnick EAThompson Mol Biol Evol 10571 (1 993)

17 G Benford Proc Natl Acad Sci USA 89 11098 (1 992)

18 OA Ryder Nature 331396 (1988) 19 K Ralls J D Ballou B A Rideout R Frankham Anim

Consen in press 20 RlKEN Gene Bank (wwwrtcrikengojp) American

Type Culture Collection (wwwatccorg) 21 Millennium Seed Bank (wrbgkeworgukseedbank

msbhtml) 22 List of Threatened Animals Wildlife Conservation and

Monitoring Centre (wwwwcmcorguk) 23 Convention on Biological Diversity (wbiodivorg

chmconvdefaulthtm) 24 Japanese Ministry of Agriculture Forestry and Fish-

eries (httpbankdnaaffrcgojp) 25 Missouri Botanical Garden St Louis MO USA

(wwwmobotorglMOBOTresearchDNAdocsl dnabankhtml)

26 This initiative is recognized as part of the Interna- tionalYear of the Biosphere (IBOY) an activity of DI- VERSITAS a creation of UNESCO and the Interna- tional Council of Scientific Unions (ICSU) and forms part of the effort to engender international coopera- tion in research and decision-making as a critical ele- ment for solving global environmental problems such as the accelerating loss of biodiversity We thank j Soberon R Medellin and an anonymous reviewer for helpful comments and suggestions

wwwsciencemagorg SCIENCE VOL 288 14APRIL 2000 277