Genetic Aspects of Rarity and Endangerment Covered many aspects in discussion of vortices

and PVAs Reserve readings provide solid background on

techniques and types of questions that are important

I’ll fill in a few more details– Genetic diversity

– Reduction in Ne

– Unique applications of genetics to conservation

Inbreeding Depression (Keller and Waller 2002)

‘Inbreeding’ is used to describe various related phenomena that all refer to situations in which matings occur among individuals that have variously similar genotypes (relatives). As conservation biologists we are concerned where this reduces genetic variability or otherwise reduces fitness (inbreeding depression).

How to Measure Inbreeding?

Keller and Waller 2002

Endangered Species Have Lower Genetic Diversity than Non-endangered Species

Haig and Avise 1996 DNA band sharing

inferred from fingerprinting

All data from birds

Inbreeding and Endangerment--Cause and Effect?

Typical early studies suggested that endangered species are genetically impoverished

Sonoran topminnow (Vrijenhoek et al. 1985)– isolated populations in desert southwest are

genetically much less diverse than widespread Mexican populations

– Recommend restocking from most diverse populations– But no direct link to suggest genetic impoverishment

caused endangerment--rather it likely resulted from it!

Effects of Inbreeding in the Wild

Deer Mice (Jimenez et al. 1994)– captured in wild and inbred or not in lab– n=367 inbred and n=419 noninbred released– -inbred survived at rate only equal to 56% of

noninbred– inbred lost weight after release, noninbred

maintained weight

Demonstrated effects of inbreeding in wild populations (Caro 2000)

Species History of Low Heterozygosity

Current inbreeding? Effects

European Adder Recent Yes Small litters, deformed young

Song sparrow Occasional Some Differential loss in cold weather

Sonoran Topminnow Recent Yes High mortality, slow growth

Florida Panther Recent Yes Testicular dysfunction

Ngorongoro lion Very recent Yes Reduced yearling production

White-footed mouse Recent Some (experimental) Lower survival, male weight loss

Cheetah Long No Sperm abnormalities

Glanville fritillary butterfly

Recent Yes Low survival, reduce egg hatching

Wide survey of inbreeding effects (Keller and Waller 2002)

Genetic Rescue of Greater Prairie Chickens (Westemeier et al. 1998)

2000 chickens in 1962---only <50 in 1994 Genetic diversity was low and fitness poor Translocated chickens from large, diverse population (MN, KS,

NE) in 1994

Fecundityrises aftertranslocation

Inbreeding Effects in Cheetah??

Low genetic variation (near clones) was associated with poor reproduction in captivity (O’Brien et al. 1985)

– low sperm count, low fecundity, low conception, high infant mortality

Classic signs of inbreeding– seems not the case!

• Reproduction in wild is fine, but cubs are lost through predation to lions and hyenas (Caro and Laurenson 1994)

• poor husbandry was likely source of poor reproduction in captivity

Reasons for Cheetah declines

Human population increase Direct killing by pastoralists Direct killing by farmers Overhunting of ungulate prey

(Caro 2000)

Black Robins Defy Genetic Bottlenecks (Ardern and Lambert 1997)

Current population of 200 birds was derived from a SINGLE breeding pair– bottleneck down to n=5 in

1980, persistence as a small population for 100 years

Minisatellite DNA variation non-existent

But, reproduction and survival is normal

Black Robin Bush Robin

Individuals (columns)nearly identical!

Recent bottleneck, but nothistorical small population

Does Genetic Variation Matter? For commonly measured variation (multilocus

heterozygosity) it does not appear to matter– DNA fingerprinting, mtDNA, etc.– Britten (1996)

• meta-analysis of 22 correlations between heterozygosity and fitness surrogates (growth rate, developmental stability

– no significant relationship

– loci measured with molecular techniques are typically neutral in the eye of evolution

– only a small sample of actual loci are measured

Could Inbreeding be Good?

Purging (Keller and Waller 2002)

– Simple population genetics models predict that the increased homozygosity resulting from inbreeding will expose recessive deleterious alleles to natural selection, thereby purging the genetic load

– Further inbreeding would then cause little or no reduction in fitness.

– Studies of purging are inconclusive in demonstrating consistent, positive effects

– Purging may only work under limited conditions• Strong deleterious effect, isolation precludes reintroduction of

deleterious alleles by immigration, inbreeding is gradual

Do Molecular Techniques Measure the Right Genes? Mitton (1994) points out that variation detected by molecular

techniques (DNA) does not correlate with fitness like variation measured at polymorphic protein loci (protein electrophoresis)– metabolism, growth rate, and viability are correlated with protein variation

Fleischer (1998) points out that quantitative genetics measures variability in traits under multilocus control by measuring heritability– measure variability in potentially important traits like body size or clutch size

Lynch (1996) details the potential importance of quantitative genetics to conservation biology

Quantitative Genetics

Measures and develops theory about heritability (in addition to other concepts)– how genotype influences phenotype and how

genotypes change through time (evolution)

Molecular genetics measures variation in loci, most of which are neutral with respect to evolution (do not affect fitness or even phenotype)

What is Heritability?

Heritability (Lynch 1996)

– fraction of phenotypic variance that has an additive genetic basis

• how much you can expect a trait to change in the next generation when selection acts on it in the present generation

– the ability to respond to novel selective challenges if proportional to the heritability of a trait

Do Heritable Traits Correlate with Fitness? Perhaps not in a simple way

– body size in Pinyon Jays is heritable (parent and offspring mass is correlated), but not directly related to survival or reproduction (Marzluff and Balda 1988)

But it is a fundamental LAW that heritability determines the ability of a population to evolve– change in mean phenotype=h2S

• h=heritability; S = selection differential

• evolution is determined by selection and inheritance

Species Can have Low Heterozygosity but High Evolutionary Potential

heterozygosity (variation at molecular level) is produced by mutation (rate of 10-8 - 10-5 per year)

heritability (variation in quantitative traits) is introduced at rate of 10-3-10-2 per generation– If population goes through a bottleneck and looses both sources

of variation, heritability recovers more quickly.• Species can have low molecular variation, but high

heritability (hence high ability to evolve)– Cheetahs are an example of this.

– Lack of heterozygosity does not mean lack of evolutionary potential

General Principles Relevant to Conservation (Lynch 1996)

Genetic variance is determined by interplay of selection, drift, and mutation– when population size is constant and selection

is constant then mutation balances drift which sets up an equilibrium level of variation

– drift reduces variation at rate of 1/(2Ne) per generation as discussed earlier

– mutation adds variation at 2m per generation

Relationship of Population Size to Evolutionary Potential When Ne < few hundred, selection is unimportant

– selection effects are spread over many loci that control a single character so effect on any 1 locus is swamped by drift

– genetic variation in heritable characters equals 2Ne 2m

• doubling population size leads to doubling in heritable variation or doubling the evolutionary potential of the population

When Ne > 1000, then drift is inconsequential– balance between mutation and selection drives variation

(evolutionary potential)

– variation is independent of population size

How Many Individuals do We Need to Get Ne > 1000? 5,000 to 10,000 (Lynch 1996)

– Ne usually is .1 to .3census N

generationper size populationN ;1

....111

progenyin variance;2

4

femalesN males, N ;

41

41

1

21

22

fm

te

e

fm

e

NNNtN

NN

NN

N

Mutational Meltdown (Lynch et al.

1993) Same as f-vortex

– drift becomes more important as population declines to very small size

– drift begins to act synergistically with accumulation of deleterious mutations

• for flies when Ne<few dozen, extinction occurs in 10-few hundred generations without stochasticity

• extinction occurs an order of magnitude or more faster with demographic or environmental stochasticity

Is Adding Individuals from Captive Propagation Beneficial? Increase in numbers, but also may upset genetic

adaptation to local conditions– esp. likely if use non-native stock

• hatchery fish, yellowstone wolves

– accentuated by long periods of selection in captivity

• develop deleterious behavior with genetic component

Also relevant when considering inducing migration between isolates– human activity fragments habitat and sets up unique selective

regime in different fragments

Unique Genetic Applications

Fleischer’s (1998) look to the future– may be able to completely type the genotype of

many organisms quickly– Genetic engineering

• add genes for disease resistance

• add genes for parasitic egg recognition

• clone old individuals to keep them in breeding population

Bessie and Noah (Seattle Times Oct. 9, 2000)

DNA from a cow egg (Bessie) was fused with skin cell from a living Asian Guar to create an embryo (Noah) that was implanted back into Bessie for gestation– Cloned Guar that does not produce immunologic

rejection in cow

“This is no longer science fiction. It’s very real” (Lanza, author of this study published in Cloning)

Using Genetics to Guide Recovery Red Wolves in SE United States (Roy et al. 1996)

Are they a basal canid or a recent hybrid?– Listed because they were believed to be a native species

from Pleistocene that was ancestral to coyotes and gray wolves

– Mitochondrial and nuclear DNA suggest red wolves are result of hybridization between gray wolves and coyotes--timing of this is uncertain

– Reintroduction sites should be selected that are in areas with few coyotes to reduce future hybridizing

Effects of Forest Loss on Squirrel Genetics

(Hale et al. 2001)

Thoughts from Lande (1999)

Evaluates Extinction Risk from stochastic, deterministic, and genetic factors– Deterministic declines in population due to human factors (habitat

loss, invasive species, climate change, etc.) are more important than stochastic factors in causing species declines

– Very large populations (>5000) may be needed to maintain rare alleles such as those needed to resist new diseases

– Once populations are small:• Inbreeding depression is most severe when population declines have

been rapid (little purging occurred), but it is easily reversed with minimal migration (1 unrelated individual joins each population every 1 or 2 generations)

• Small populations with low fitness may go extinct from fixation of new deleterious mutations. But even very small populations with high fitness rarely suffer from fixation of deleterious mutations.

References Haig, SM and JC Avise. 1996. Avian conservation genetics. PP160-189 In. JC Avise and

JL Hamrick (ed.) Conservation genetics. Chapman & Hall. New York. Lynch, M. 1996. A quantitative-genetic perspective on conservation issues. PP 471-501

In. JC Avise and JL Hamrick (ed.) Conservation genetics. Chapman & Hall. New York. Britten, HB. Meta-analyses of the association between multilocus heterozygosity and

fitness. Evolution 50:2158-2164. Fleischer, RC. 1998. Genetics and avian conservation. PP 29-47 In. JM Marzluff and R

Sallabanks (eds.) Avian Conservation. Island Press. Covelo, CA. Mitton, JB. 1994. Molecular approaches to population biology. Ann. Rev. Ecol. Syst.

25:45-69 Lynch, M. R. Burger, D. Butcher, and W. Gabriel. 1993. The mutational meltdown in

asexual populations. J. Heredity 84:339-344. Westemeier, R. L., Brawn, J. D., Simpson, S. A., Esker, T. L., Jansen, R. W., Walk, J.

W., Kershner, E. L., Bouzat, J. L., and K. N. Paige. 1998. Tracking the long-term decline and recovery of an isolated population. Science 282:1695-1698.

More References Ardern, S. L. and D. M. Lambert. 1997. Is the black robin in genetic peril?

Molecular Ecology 6:21-28 Caro, T. M. and M. K. Laurenson. 1994. Ecological and genetic factors in

conservation: a cautionary tale. Science 263:485-486. Jimenez, J. A., K. A. Hughes, G. Alaks, L. Graham, and R. C. Lacy. 1994. An

experimental study of inbreeding depression in a natural habitat. Science 266:271-273.

O’Brien, S.J., Roelke, M. E., Marker, L., Newman, A., Winkler, C. A., Meltzer, D., Colly, L., Evermann, J. F., Bush, M., and D. E. Wildt. 1985. Genetic basis for species vulnerability in the Cheetah. Science 227:1428-1434.

Roy, M. S., E. Geffen, D. Smith, and R. K. Wayne. 1996. Molecular genetics of pre-1940 red wolves. Conservation Biology 10:1413-1424.

Vrijenhoek, R. C., M. E. Douglas, and G. K. Meffe. 1985. Conservation genetics of endangered fish populations in Arizona. Science 229:400-402.

Still More Refs Hale, ML, Lurz, PWW, Shirley, MDF, Rushton, S., Fuller, RM, and

K. Wolff. 2001. Impact of landscape management on the genetic structure of red squirrel populations. Science 293:2246-2248.

Caro, T. 2000. Controversy over behavior and genetics in Cheetah conservation. In. LM Gosling and WJ Sutherland, eds. Behavior and Conservation.

Keller, LF and DM Waller. 2002. Inbreeding effects in wild populations. Trends in Ecology and Evolution 17:230-241.

Lande, R. 1999. Extinction risks from anthropogenic, ecological, and genetic factors. Pp 1-22. In Genetics and the Extinction of Species (Landweber, LF and AP Dobson, eds.). Princeton University Press