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Teachers' Guide ­ 7th Grade Life Sciences

School Outreach Program

BOTTLENECK GENES

Species Conservation: Black-Footed Ferret

Fourth Edition (2009) 2008 Revision: Ricki Ferrence & Kate Christen 2003 Revision: Vanessa Neuerburg Developed by: Susan R. Peachey Jennifer L. Buff CRC Education Program Manager [email protected]

©2000-2009, Conservation & Research Center, Smithsonian Institution's National Zoological Park

BOTTLENECK GENES

Species Conservation: Black-Footed Ferret for Virginia 7th Grade Life Sciences Students

TABLE OF CONTENTS

Topics Corresponding Virginia Science Standards of Learning (for 7th grade life science) In-Class Program: Duration, Class Size Goal Objectives Overview Pre-program Preparation Classroom Procedure and Activities Black-Footed Ferret Facts Vocabulary List Student Worksheet Additional Internet Resources and Scientific Publications 2 2

2 2 2 2-3 3 3-4 5-8 9-11 12-13 14-15

Construction of the black-footed ferret mobile display unit was funded by the National Fish and Wildlife Foundation and Black-footed Ferret Recovery Foundation

This program and publication received federal support from the Smithsonian Latino Center

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BOTTLENECK GENES Species Conservation: Black-Footed Ferret Topics:

Genetic diversity, small population biology and endangered species

Corresponding Seventh Grade Virginia Science Standards of Learning (SOLs):

Bold elements are highly emphasized in this program.

LS.5, LS.7, LS.8, LS.9, LS.10, LS.11, LS.12, LS.13, LS.14 In-Class Program: Duration: 55 minutes

Class Size: Up to 25 students

Goal:

To acquire knowledge about small population biology, genetic diversity, and the impact of genetic bottlenecks on species conservation.

Objectives:

Through an interactive activity, students are introduced to the study of conservation genetics and population bottlenecks. They will discover how the loss of genetic diversity and genetic characteristics can affect a population's ability to respond to changes in its environment. Other topics covered include: (1) wildlife management issues, and (2) the role of science and technology in conservation. Following this program, students will: 1. Understand concepts related to small population biology and genetic diversity as it pertains to conservation of endangered species. 2. Discover how the loss of genetic diversity in a species can affect a population's ability to respond to changes in its environment. 3. Explain the role that science and technology can play in conservation efforts. 4. Be familiar with one of the most endangered species in North America, the blackfooted ferret.

Overview:

This module has two sections: In section one, an overview/discussion will provide an introduction to the natural history of the black-footed ferret, including: (1) a review of the black-footed ferret's unique niche in the prairie ecosystem, (2) issues leading to its decline, and (3) current conservation initiatives (including programs at the Conservation & Research Center). Basic information on genetic diversity and the role genes play in natural selection and adaptation will also be discussed. Special emphasis will be placed on the effects of fragmentation on small population biology. In section two, students will participate in an interactive genetic bottleneck activity. Student teams, representing black-footed ferret populations, will receive a random number of colored beads, literally through the neck of a bottle. These beads represent the genes found in their

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hypothetical population of black-footed ferrets, following a genetic bottleneck event. Student teams will also receive five cards from a deck of numbered cards, each one corresponding to a series of environmental situations. Using the genes (beads) and environmental factors (numbered cards), student teams perform the following tasks: 1. Calculate the percent genetic diversity of their population. 2. Use a key found on the student worksheet to identify the genetic characteristics their population received as well as the genes lost after a genetic bottleneck event. 3. Write a prediction for the ferrets' survival, based on the population's genetic make-up and the environmental situations presented to the population. Students will document their thoughts on whether their hypothetical black-footed ferret population has the genetic characteristics necessary for adapting to random changes in their environment.

Pre-Program Preparation:

This outreach program is meant to support the genetics instruction at the middle school level (7th grade Virginia Life Sciences Standards). Students will receive a greater benefit from the program if they prepare by reviewing vocabulary terms and concepts provided in this guide, prior to the scheduled program. Additionally, if the program includes a visit from the CRC Ambassador black-footed ferret, students should be reminded that in the presence of a living wild animal, they need to remain calm and quiet. Teachers must remain on hand to assist the CRC facilitator with student supervision. Classroom set-up and supplies are brought by CRC staff; teachers must ensure that each child is already provided with a pencil to use during the activity. CRC facilitator will supply: PowerPoint presentation, along with computer and LCD projector; student worksheets; bottleneck activity components; animal skulls.

Classroom Procedure and Activities (est. time ­ 55 minutes):

Activity One: Overview presentation and discussion A powerpoint presentation introduces students to the history of the black-footed ferret and prairie ecosystem. Current conservation initiatives are described, and the role that genetics research plays in restoring threatened populations is explained. At a break in the presentation, CRC educator will use a glass bottle with colored beads to explain the concept of a "bottleneck effect" or "genetic bottleneck." Bottleneck effect: When a population experiences a severe change that kills off many individuals, the survivors represent only a portion of the original genetic diversity. The subsequent diversity of genes, and associated genetic characteristics or traits, are limited by the bottleneck event. Activity Two: Genetic bottleneck demonstration Review concepts of genetic diversity and population bottlenecks. Class is divided into teams of two to three students each, and each team is given a copy of the student worksheet and bottleneck key.

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Each team receives a small handful of colored beads from the bottle (colors represent genetic characteristics of the team's hypothetical black-footed ferret population, after a genetic bottleneck event). Teams match colors to the key to document the genetic characteristics of their population. Teams randomly select five cards from a deck of "environmental change" cards. Using the key, teams match the numbered cards selected with the environmental scenarios represented by each number. On the student worksheet, teams: 1. Calculate the percent genetic diversity for their hypothetical black-footed ferret population, based on the number of characteristics (colors of beads) they received through the bottleneck 2. Describe their population based on its current genetic makeup 3. Develop and write a scenario for their population's survival, addressing the following: · How well is your population genetically equipped to survive in its environment? · How do random changes in the environment affect the population? · Does a high or low percent genetic diversity affect your population's ability to survive changes in its environment? 4. Teams present results to the class for discussion and questions

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Black-Footed Ferret Facts (May 2007)

Phylogeny: This ferret species is a member of the weasel family, Mustelidae, along with the badger, fisher, marten, otter, mink, wolverine and weasel. There are three species of wild ferrets: 1. Black-footed ferret (Mustela nigripes) 2. European polecat (Mustela putorius) 3. Siberian polecat (Mustela eversmanni)

The black footed ferret is the only wild ferret native to North America. Once considered the rarest mammal in North America, it remains endangered. The domestic ferret (Mustela putorius furo), also found in North America, is a different species; it is a descendant of the European polecat. Habitat: · North American Great Plains, from southern Saskatchewan, Canada to northern Mexico · Grasslands ecosystem · Anywhere you find prairie dogs (must have prairie dog towns to survive) · Solitary except mother with her babies (called "kits") Description: · 20 to 24 inches long · Males weigh about 1 kg (2.2 lbs) · Females are smaller and weigh about 800 grams (0.8 kg; 1.8 lbs) · Black mask, feet and tipped tail

Black-footed ferret at the National Zoo

Red Tailed Hawk

Lifespan: · In the wild, black footed ferrets can live two to three years · In captivity, black footed ferrets can live five to seven years Predators: · Badgers · Coyotes and swift foxes · Owls, eagles and other birds of prey · Snakes

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Diet: · Considered a "specialist carnivore" (prairie dog equals 90% of its diet) · Will kill and eat prairie dog and then live in prairie dog burrows · Nocturnal carnivore Breeding: · Seasonal breeders (March-June) · Females come into estrus (heat) only once a year (similar to giant pandas) · Average litter size = three kits Both male and female are able to breed and produce offspring at one year of age Females produce offspring for first three years; fertility declines after three years of age Males produce sperm from maturity until death Events leading to endangerment: · Habitat lost due to agriculture, industrial growth and urban development · Eradication of prairie dogs, with government aid · Disease: Sylvatic plague: similar to bubonic plague; transmitted by fleas; infects prairie dogs and ferrets directly; ferrets can also be infected by eating infected prairie dogs. Canine distemper: dogs and other canids are carriers; ferrets are highly susceptible

· · ·

1,601 prairie dogs poisoned in one day on one acre of land in 1919 in Arizona

Decline of black-footed ferrets in the wild: Over the last century, populations of black-footed ferrets began to decline. A small population in Mellette County, South Dakota, was studied by the U.S. Fish and Wildlife Service from 1964 to 1974. Twenty of the 151 prairie dog colonies were inhabited by blackfooted ferrets, and during this time it became evident that black-footed ferrets were dependent on large colonies of prairie dogs. In 1966, the Endangered Species Preservation Act was passed, and in 1967, the blackfooted ferret was declared an endangered species. In 1971, six ferrets were brought to the U.S. Fish and Wildlife Service Research Center in Patuxent, MD, to initiate a captive breeding program; however, these first attempts at captive breeding proved unsuccessful and the last captive black-footed ferret died in January 1979. By the mid-70's, the black-footed ferret was thought to be extinct. A fortunate discovery: In 1981, a dog named Shep killed an animal on a ranch in Meeteetse, Wyoming. Shep's owner took this animal to a taxidermist for identification, and it turned out that it was a black footed ferret! This precipitated the discovery of the last known wild population of black footed ferrets.

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This newly-discovered population peaked at around 130 animals in 1984, but then declined. In 1985, outbreaks of both canine distemper and sylvatic plague further decimated the population. Between 1985 and 1987, the last 18 black-footed ferrets were brought into a captive breeding facility near Laramie, WY in a last-ditch effort to keep the species from going extinct. This first facility in Wyoming became the National Black-Footed Ferret Conservation Center, and is managed by the U.S. Fish and Wildlife Service. This facility was subsequently moved to Carr, Colorado (near Fort Collins) and houses approximately 60% of all captive black-footed ferrets. Other facilities joined the breeding program, including: · Smithsonian's National Zoo, Conservation and Research Center, Front Royal, VA · Henry Doorly Zoo, Omaha, NE (now not in program) · Toronto Zoo, Toronto, Canada · Phoenix Zoo, Phoenix, AZ · Louisville Zoo, Louisville, KY · Cheyenne Mountain Zoo, Colorado Springs, CO Recovery Goals: The goal of the 1988 Black-Footed Ferret Recovery Plan is to provide sufficient animals for reintroduction and recovery of black-footed ferrets in the wild, while maintaining a selfsustaining captive population. The Plan emphasizes natural breeding, as well as the development of assisted reproductive techniques (such as artificial insemination). Between 1987 and 2007, more than 6,000 kits have been born in the captive-breeding program. The captive population size at the beginning of the 2007 breeding season was 271 animals (108 males; 163 females). Reintroduction: The 1988 Recovery Plan called for establishing at least 1,500 breeding adults in ten wild populations by 2010. The captive-breeding program has been successful at producing a high number of black-footed ferrets for reintroduction. Over 2,500 ferrets have been released since 1991. It was estimated that in 2006 there were 850 black-footed ferrets surviving in the wild. While much progress has been made, the fate of the species still hangs in the balance, as the prairie ecosystem continues to vanish. Persistent political and social issues also hamper recovery efforts. Reintroduction sites as of 2007 (and the year they were established): · · · · · Shirley Basin, WY (1991) Charles M. Russell National Wildlife Refuge, MT (1994) Conata Basin/Badlands National Park, SD (1994/1996) Aubrey Valley, AZ (1996) Fort Belknap Indian Reservation, MT (1997) · · · · · · · Coyote Basin, UT (1999) Bureau of Land Management 40 complex, MT (2000) Janos, Mexico (2000) Cheyenne River Sioux Tribe, SD (2001) Northwest/Wolf Creek CO (2001) Rosebud Sioux Tribe, SD (2004) Lower Brule Sioux Tribe, SD (2006)

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Smithsonian's National Zoo, Conservation and Research Center (CRC), Front Royal, Virginia: CRC has one of the world's most extensive programs in conservation biology research, training and education. Because of the unique facilities and limited public access, CRC became the first USFWS partner in the captive breeding program, in 1988. The 1988 Black-Footed Ferret Recovery Plan emphasized natural breeding to maintain the captive individuals, but it also recognized the potential benefits of assisted reproductive technology, especially artificial insemination (AI). Scientists from CRC started studying the basic biology of the domestic ferret and the Siberian polecat to develop techniques that could be applied to the blackfooted ferret. Milestones: In 1995, it was discovered that more than 50% of the black-footed ferret males had failed to sire offspring due to a combination of behavioral and physiological factors, but sperm quality was not compromised. In 1996, scientists at the Conservation and Research Center began using artificial insemination in black-footed ferrets to maintain genetic diversity. Laparoscopy is used to visualize the reproductive tract; then sperm is deposited directly into the uterus. For artificial insemination, semen can be collected from a male or frozen/thawed semen stored in the Black-Footed Ferret Genome Resource Bank (repository of frozen sperm) can be used. · · · From 1988 through 2006, 354 kits were born from natural breeding at CRC. From 1996 to 2004, 133 kits were born from artificial insemination. Since 1991, over 200 black-footed ferrets from the National Zoo's Conservation and Research Center have been released into the wild.

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Bottleneck Genes Species Conservation: Black-Footed Ferret VOCABULARY LIST

adaptations - the ways in which living things have adjusted to their environment through biology or behavior, thereby improving their chances of survival behavior - anything an organism does that involves action or response biological diversity - the richness and variety of life forms in a given ecosystem, or of the entire Earth; also called biodiversity bottleneck effect - when a population experiences a severe change that kills off many individuals, the survivors retain only a portion of the original genetic diversity. The consequent diversity of genes, and associated genetic characteristics or traits of the new population are thus limited by the effect of this "genetic bottleneck" event camouflage - body colors or patterns that allow an animal to blend into its surroundings carnivore - a flesh-eating animal or predatory organism (such as an insectivorous plant) coloration - the arrangement of color and markings on a particular species; coloration often serves a protective function community - a group of interdependent organisms inhabiting the same region and interacting with each other (see ecosystem) conservation biology ­ a field of science focused on investigating, and endeavoring to protect, Earth's biodiversity, including populations and species that have been affected by habitat loss, exploitation, and/or environmental change. Research results are applied to the formulation and implementation of informed decisions to ensure the future of the Earth's biodiversity, including survival of specific populations and species. conservation genetics ­ a field of science which investigates the extent of diversity among the individuals in a population and/or species and, based upon this information, designs management techniques intended to ensure the survival of the population/species, dominant gene ­ a gene that always shows its effect, or expression, in an organism, even if a corresponding recessive gene is also present ecosystem - a unit consisting of all the living organisms in a given area (the community), as well as their relationship to the non-living (abiotic) surrounding environment. Thus, an ecosystem's components may include plants, animals, and microorganisms, soil, rocks, and minerals, water sources, and atmosphere endangerment - a species' exposure to the threat of extinction epidemic ­ a contagious disease that spreads widely and rapidly, affecting many individuals within a population or area at the same time eradication ­ complete removal or destruction

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evolution - a biological process that results in heritable genetic changes in a population spread over many generations. To quote evolutionary biology Douglas Futuyma (Evolutionary Biology, Sinauer Associates 1986), "Biological evolution . . . is change in the properties of populations of organisms that transcend the lifetime of a single individual. The ontogeny [life cycle] of an individual is not considered evolution; individual organisms do not evolve. The changes in populations that are considered evolutionary are those that are inheritable via the genetic material from one generation to the next. Biological evolution may be slight or substantial; it embraces everything from slight changes in the proportion of different alleles [alleles=varieties of genes that code for a particular trait] within a population (such as those determining blood types) to the successive alterations that led from the earliest protoorganism to snails, bees, giraffes, and dandelions." extinction - the eradication of a species from Earth food chain - a chain of organisms that are linked together because each is food for the next in line; all of the food chains found in an ecosystem are called a food web. founder effect -the effect of the establishment of a new population by only a small number of individuals, carrying only a small fraction of the original population's genetic variation gene - a piece of DNA that codes for a particular trait; the basic unit of heredity gene pool - all the genes present in a given population at a particular time generalist - a very adaptable species with a flexible diet, and high birthrate, that can thrive in a wide variety of habitats genetic diversity - variation in the genes found in individuals within a population of a single species, and the pattern of genetic variation found within different populations of the same species genetic erosion - loss of genetic diversity between and within populations of the same species over time; or reduction of the genetic basis of a species due to human intervention, environmental changes, and similar factors. genetics - the science of heredity and variation in living organisms, incorporating the study of the genetic material responsible for inherited traits habitat - a place providing appropriate living conditions for an organism, species, or community herbivore - an animal whose diet consists almost exclusively of plants heredity - the genetic transmission of particular characteristics or traits from one generation to the next inbreeding - mating of closely related individuals within a species. This behavior limits the genetic combinations possible in offspring, leading to reduction in genetic diversity and potentially reduced health and lower levels of fertility for the species Mustelidae ­ a large and diverse taxonomic family of fur-bearing carnivores, including the weasel, badger, wolverine, otter, fisher and ferret; commonly referred to as the weasel family niche ­ in ecological terms, an organism's role, or job, in an ecosystem nocturnal - active during the night, rather than during daylight hours

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omnivore - an animal that eats both plants and animals population - all the individuals of one species that occupy the same given area at the same time range - the geographic region in which a particular plant or animal is found (e.g., the Great Plains of the Western US and Mexico) recessive gene ­ a gene whose expression is repressed when the dominant gene is present reintroduction ­ the effort to prevent the extinction of threatened species and populations by deliberately releasing them into the wild to areas where they were native but from which they have disappeared or become extirpated in historic times reproduction - the sexual or asexual process by which organisms generate others of the same kind rodent - any of the single largest order of mammals (Rodentia), including prairie dogs, rats, squirrels, and beavers; characterized by constantly growing incisors adapted for gnawing or nibbling specialist - a species that is primarily dependent on a single food source and/or habitat survival - the process of remaining alive or in existence; in species terms, survival entails that sufficient individuals live to maturity and reproduce

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BLACK-FOOTED FERRET

Genetic Bottleneck Scenario

Team member names:

Step 1: KEY TO GENETIC CHARACTERISTICS

Instructions: Using the color code key below (bead color = genetic characteristic), circle the genetic characteristics your hypothetical black-footed ferret population received through the genetic bottleneck event. Then answer the questions related to genetic diversity, bottleneck events, and characteristics. BLACK ... precise vision ORANGE ... accurate smell RED ... healthy reproduction PINK ... strong claws / legs WHITE ... immunity to canine distemper PURPLE ... acute hearing GREEN ... agility YELLOW ... camouflage DARK BLUE (B)* ... healthy jaw formation (dominant gene) LIGHT BLUE (b)* ... jaw deformity (recessive gene) * Guidelines for documenting the expression of dominant and recessive genes: 1. BB = dominant gene expressed 2. Bb = dominant gene expressed 3. bb = recessive gene expressed

Questions about genetic characteristics following a bottleneck event: 1. Calculate the percent (%) genetic diversity of your hypothetical black-footed ferret population. 10 genes (colors) represent 100% genetic diversity in the original black-footed ferret population. a. ______ genes (colors) received / 10 original genes in the population = _______ (decimal) b. Multiply this decimal amount by 100 = _______ % 2. How was your population affected by dominant and recessive genetic characteristics?

Step 2: KEY TO 16 ENVIRONMENTAL SITUATIONS

Instructions: Using the key below (card number = environmental situation), circle the five situations that took place in the locality where your hypothetical black-footed population lives. Some environmental situations may relate directly to your population's genetic characteristics, others may be random environmental events where your population's genetic characteristics allow adaptations to changes. 1. A farmer tries to protect his wheat fields by exterminating resident prairie dogs. 2. The survival rate of this year's baby black-footed ferrets is high, and as the babies grow into adulthood, they will disperse from your population into adjacent prairie dog towns to establish a new colony. 3. Humans building homes 10 miles away wiped out a prairie dog colony and the surviving black-footed ferrets from there invade your territory for food. 4. Female ferrets in your population can only produce one kit per year unless they have the gene for a healthy rate of reproduction. 5. Ranchers allow their dogs to run loose (hint: domestic dogs carry dog diseases). 6. A new generation of captive-born black-footed ferrets is released at a nearby reintroduction site.

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7. Sylvatic plague strikes the resident prairie dog colony; there is an 80% prairie dog mortality rate. 8. A coyote prowls at night. A good sense of smell would allow you to avoid this crafty predator. 9. A black-footed ferret will need healthy, strong jaws in order to hang on and win the fight as its aggressive prairie dog prey fights back in its dark, narrow, winding burrow system. 10. A great horned owl relies on its keen eyesight to spot potential prey in the dark. Can your black-footed ferrets remain unseen? 11. A badger sneaks around the prairie dog town. Can your black-footed ferrets hear it coming with enough time to flee? 12. A prairie dog colony is established on a nearby Native American reservation. 13. Severe rains flood the prairie dog burrows. 14. An interstate is built nearby. 15. Drought causes the prairie soil to compact and harden. Black-footed ferrets will need strong legs in order to adapt the burrows stolen from their prairie dog prey to make their homes. 16. A golden eagle hunts for a meal. Good vision would help your ferrets avoid capture. Step 3: POPULATION PREDICTIONS Instructions: Using the table that that follows, predict your population's chances of survival for each of your environmental situations. Consider, specifically, how your population's genetic makeup impacts your population's ability to adapt to each situation. Environmental Situation # Survival Prediction (good/poor) Reasons (explain your prediction by describing the characteristics that either help or hinder your population's survival)

Overall thoughts on the survival chances of your black-footed ferret population:

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Bottleneck Genes Species Conservation: Black-Footed Ferret ADDITIONAL INTERNET RESOURCES AND SCIENTIFIC PUBLICATIONS

Visit these websites for more in-depth information: http://nationalzoo.si.edu/Animals/NorthAmerica/Conservation/blackfootedferrets/

The Smithsonian's National Zoo's black-footed ferret website features a video providing an overview of the plight of the black-footed ferret and of the Zoo's involvement with its recovery program, along with related resources for further investigation. Classrooms may "adopt-a-black-footed-ferret" to help support the Zoo's world-class services to black-footed ferrets, including medical care and habitat improvement.

www.blackfootedferret.org

This website was created by the Black-footed Ferret Recovery Implementation Team (BFFRIT). The BFFRIT was established in 1996 to integrate more effectively the expertise and resources of those contributing to the black-footed ferret's recovery. Led by the U.S. Fish and Wildlife Service (USFWS), this multi-organization effort includes representatives from federal and state governments, zoos, and nonprofit organizations. The team was created pursuant to Section 4(f)(2) of the amended Endangered Species Act, which authorizes the Secretary of the Interior to procure the services of appropriate public and private agencies, institutions, and other qualified persons to help implement endangered species recovery plans. Although the BFFRIT is strictly advisory, the team assists in the development of national guidance, provides recommendations to USFWS regarding the appropriate conduct, methods, and priorities for ferret recovery efforts, and reviews any revisions or updates to the black-footed ferret recovery plan.

http://files.dnr.state.mn.us/assistance/backyard/prairierestoration/goingnative.pdf

The Minnesota Department of Natural Resources has put together a beautiful publication on prairie reconstruction, called Going Native: A Prairie Restoration Handbook for Minnesota Landowners. Although intended for individuals who are returning their property to a natural state, the book is very easy to read and has wonderful photographs, quotations, and resources on general prairie information. The book can be downloaded from this web address with Adobe Acrobat Reader, or it can also be requested directly from the Minnesota DNR.

www.science.mcmaster.ca/biology/CBCN/genetics

This website is the result of a biology course taught at McMaster University (Hamilton, Ontario). "Biology Inquiry: Genetics in Conservation," is an independent study seminar course for fourth year university students. Course themes include the role of genetic individuality as the basis of biodiversity, and the use of contemporary molecular genetics methods and population genetics concepts in conservation biology. From 1997-99, students added pertinent material to the website edited by course instructor Dr. David Galbraith. Topics include: the genetics of small populations of plants and animals; inbreeding; population bottlenecks; extinction vortices; and the declining population problem. Techniques examined include DNA fingerprinting, DNA sequencing, minisatellite markers and RAPDs; case studies range from cheetahs and lions to rattlesnakes and beavers. Please contact David Galbraith ([email protected]) for more information.

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Bottleneck Genes activity in Project Wild

This activity has been adapted for use in the 2003 edition of the Project Wild K-12 Curriculum and Activity Guide. Another activity in this guide pertaining to population biology is "Birds of Prey," in which students explore the relationship between ground squirrels and falcons. For more information about Project Wild and its curriculum materials, see: http://projectwild.org/getWild.htm

Scientific Publications on conservation genetics and small population biology

Frankham, R., J. D. Ballou, and D. Briscoe. 2004. Primer of Conservation Genetics. New York: Cambridge University Press. Ballou, J. D., and T. J. Foose. 1994. Demographic and genetic management of captive populations. In Wild Mammals in Captivity. Chicago: University of Chicago Press, 263-283. Ralls, K; Brugger, K, and Ballou, J D. 1979. Inbreeding and juvenile mortality in small populations of ungulates. Science, 206: 1101-1103. Frankham, R. 1995. Conservation genetics. Annual Review of Genetics, 29: 305-327. Ebenhard, T. 1995. Conservation breeding as a tool for saving animal species from extinction. Trends in Ecology & Evolution (TREE). 10(11): 438-443.

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