Part I Introduction

PA R T I

Introduction

COPYRIGHTED MATERIAL

CHAPTER 1

Introduction

One- horned rhinoceros, Section 5.3

We are at a critical juncture for the conservation and study of biological diversity: such an opportunity will never occur again. Understanding and maintaining that diversity is the key to humanity’ s continued prosperous and stable existence on Earth. US National Science Board Committee on Global Biodiversity (1989)

The extinction of species, each one a pilgrim of four billion years of evolution, is an irreversible loss. The ending of the lines of so many creatures with whom we have traveled this far is an occasion of profound sorrow and grief. Death can be accepted and to some degree transformed. But the loss of lineages and all their future young is not something to accept. It must be rigorously and intelligently resisted. Gary Snyder (1990)

Chapter Contents

1.1 Genetics and civilization, 4 1.2 What should we conserve? 5 1.3 How should we conserve biodiversity? 9 1.4 Applications of genetics to conservation, 10 1.5 The future, 12

Guest Box 1 The role of genetics in conservation, 13

Conservation and the Genetics of Populations‚ Second Edition. Fred W. Allendorf, Gordon Luikart, and Sally N. Aitken. © 2013 Fred W. Allendorf, Gordon Luikart and Sally N. Aitken. Published 2013 by Blackwell Publishing Ltd. 4 Introduction

We are living in a time of unprecedented extinctions tion of plants is thought to have been perhaps the key (Myers and Knoll 2001 , Stuart et al . 2010 , Barnosky step in the development of civilization (Diamond et al . 2011 ). Current extinction rates have been esti- 1997 ). Early peoples directed genetic change in domes- mated to be 50– 500 times background rates and are tic and agricultural species to suit their needs. It has increasing; an estimated 3000 – 30,000 species go been estimated that the dog was domesticated over extinct annually (Woodruff 2001 ). Projected extinc- 15,000 years ago, followed by goats and sheep around tion rates vary from 5 – 25% of the world ’ s species by 10,000 years ago (Darlington 1969 , Zeder and Hess 2015 or 2020. Approximately 23% of mammals, 12% 2000 ). Wheat and barley were the fi rst crops to be of birds, 42% of turtles and tortoises, 32% of amphib- domesticated in the Old World approximately 10,000 ians, 34% of fi sh, and 9 – 34% of major plant taxa are years ago; beans, squash, and maize were domesticated threatened with extinction over the next few decades in the New World at about the same time (Darlington (IUCN 2001 , Baillie et al. 2004 ). Over 50% of animal 1969 , Kingsbury 2009 ). species are considered to be critically endangered, The initial genetic changes brought about by culti- endangered, or vulnerable to extinction (Baillie et al . vation and domestication were not due to intentional 2004 ). A recent assessment of the status of the world ’ s selection but apparently were inadvertent and inher- vertebrates, based on the International Union for the ent in cultivation itself. Genetic change under domes- Conservation of Nature (IUCN) Red List, concluded tication was later accelerated by thousands of years of that approximately 20% are classifi ed as Threatened. purposeful selection as animals and crops were selected This fi gure is increasing primarily because of agricul- to be more productive or to be used for new purposes. tural expansion, logging, overexploitation, and inva- This process became formalized in the discipline of sive introduced species (Hoffmann et al . 2010 ). agricultural genetics after the rediscovery of Mendel’ s The true picture is much worse than this because the principles at the beginning of the 20th century. conservation status of most of the world ’ s species The ‘ success ’ of these efforts can be seen every- remains poorly known. Recent estimates indicate that where. Humans have transformed much of the land- less than 30% of the world ’ s arthropod species have scape of our planet into croplands and pasture to been described (Hamilton et al . 2010 ). Less than 5% of support the over 7 billion humans alive today. It has the world’ s described animal species have been evalu- been estimated that 35% of the Earth ’ s ice - free land ated for the IUCN Red List. Few invertebrate groups surface is now occupied by crops and pasture (Foley have been evaluated, and the evaluations that have et al . 2007 ), and that 24% of the primary terrestrial been done have tended to focus on molluscs and crus- productivity is used by humans (Haberl et al . 2007 ). taceans. Among the insects, only the swallowtail but- Recently, however, we have begun to understand the terfl ies, dragonfl ies, and damselfl ies have received cost at which this success has been achieved. The much attention. replacement of wilderness by human- exploited envi- Conservation biology poses perhaps the most diffi - ronments is causing the rapidly accelerating loss of cult and important questions ever faced by science species and ecosystems throughout the world. The (Pimm et al. 2001 ). The problems are diffi cult because continued growth of the human population and their they are so complex and cannot be approached by the direct and indirect effects on environments imperils a reductionist methods that have worked so well in other large proportion of the wild species that now remain. areas of science. Moreover, solutions to these problems Aldo Leopold inspired a generation of biologists to require a major readjustment of our social and politi- recognize that the actions of humans are embedded cal systems. There are no more important scientifi c into an ecological network that should not be ignored challenges because these problems threaten the con- (Meine 1998 ). The organized actions of humans are tinued existence of our species and the future of the controlled by sociopolitical systems that operate into biosphere itself. the future on a timescale of a few years at most. All too often our systems of conservation are based on the economic interests of humans in the immediate future. 1.1 GENETICS AND CIVILIZATION We tend to disregard, and often mistreat, elements that lack economic value but that are essential to the stabil- Genetics has a long history of application to human ity of the ecosystems upon which our lives and the concerns. The domestication of animals and cultiva- future of our children depend. Introduction 5

In 1974 , Otto Frankel published a landmark paper 1.2.1 Phylogenetic d iversity entitled ‘ Genetic conservation: our evolutionary responsibility’ , which set out conservation priorities: The amount of genetic divergence based upon phylogenetic relationships is often considered when setting First, . . . we should get to know much more about the conservation priorities for different species (Mace et al . structure and dynamics of natural populations and com- 2003 , Avise 2008 ). For example, the United States Fish munities. . . . Second, even now the geneticist can play a and Wildlife Service (USFWS) assigns priority for part in injecting genetic considerations into the planning listing under the Endangered Species Act (ESA) of the of reserves of any kind. . . . Finally, reinforcing the United States on the basis of “ taxonomic distinctive- grounds for nature conservation with an evolutionary ness ” (USFWS 1983 ). Species of a monotypic genus perspective may help to give conservation a permanence receive the highest priority. The tuatara raises several which a utilitarian, and even an ecological grounding, fail important issues about assigning conservation value to provide in men’ s minds. and allocating our conservation efforts based upon taxonomic distinctiveness (Example 1.1 ). Frankel, an agricultural plant geneticist, came to the Faith (2008) recommends integrating evolutionary same conclusions as Leopold, a wildlife biologist, by a processes into conservation decision - making by con- very different path. In Frankel ’ s view, we cannot antici- sidering phylogenetic diversity. Faith provides an pate the future world in which humans will live in a approach that goes beyond earlier recommendations century or two. Therefore, it is our responsibility to that species that are taxonomically distinct deserve “ keep evolutionary options open” . It is time to apply greater conservation priority. He argues that the phylo- our understanding of genetics to conserving the genetic diversity approach provides two ways to natural ecosystems that are threatened by human consider maximizing biodiversity. First, considering civilization. phylogeny as a product of evolutionary process enables the interpretation of diversity patterns to maximize biodiversity for future evolutionary change. Second, phylogenetic diversity also provides a way to better 1.2 WHAT SHOULD WE CONSERVE? infer biodiversity patterns for poorly described taxa when used in conjunction with information about geo- Conservation can be viewed as an attempt to protect graphic distribution. the genetic diversity that has been produced by evolu- Vane - Wright et al . (1991) presented a method for tion over the previous 3.5 billion years on our planet assigning conservation value on the basis of phyloge- (Eisner et al . 1995 ). Genetic diversity is one of three netic relationships. This system is based upon the forms of biodiversity recognized by the IUCN as deserv- information content of the topology of a particular ing conservation, along with species and ecosystem phylogenetic hierarchy. Each extant species is assigned diversity ( www.cbd.int , McNeely et al . 1990 ). Unfortu- an index of taxonomic distinctness that is inversely nately, genetics has been generally ignored by the proportional to the number branching points to other member countries in their National Biodiversity Strat- extant lineages. May (1990) has estimated that the egy and Action Plans developed to implement the Con- tuatara (Example 1.1 ) represents between 0.3 and 7% vention on Biological Diversity (CBD) (Laikre et al . of the taxonomic distinctness, or perhaps we could 2010a ). say genetic information, among reptiles. This is equiva- We can consider the implications of the relationship lent to saying that each of the two tuatara species between genetic diversity and conservation at many is equivalent to approximately 10 to 200 of the levels: genes, individuals, populations, varieties, sub- ‘ average ’ reptile species. Crozier and Kusmierski species, species, genera, and so on. Genetic diversity (1994) developed an approach to setting conservation provides a retrospective view of evolutionary lineages priorities based upon phylogenetic relationships and of taxa (phylogenetics), a snapshot of the current genetic divergence among taxa. Faith (2002) has pre- genetic structure within and among populations (pop- sented a method for quantifying biodiversity for the ulation and ecological genetics), and a glimpse ahead purpose of identifying conservation priorities that con- to the future evolutionary potential of populations and siders phylogenetic diversity both between and within species (evolutionary biology). species. 6 Introduction

Example 1.1 The t uatara: a living f ossil

The tuatara is a lizard- like reptile that is the remnant and indicate that fewer than 300 individuals of this of a taxonomic group that ﬂ ourished over 200 million species remain on a single island, North Brother Island years ago during the Triassic Period (Figure 1.1 ). in Cook Strait. Another population of S. guntheri Tuatara are now conﬁ ned to some 30 small islands off became extinct earlier in this century. Daugherty et al . the coast of New Zealand (Daugherty et al . 1990). (1990) argued that not all tuatara populations are of Three species of tuatara were recognized in the 19th equal conservation value. As the last remaining popu- century. One of these species is now extinct. A second lation of a distinct species, the tuatara on North species, Sphenodon guntheri , was ignored by legisla- Brother Island represent a greater proportion of the tion designed to protect the tuatara which ‘ lumped’ all genetic diversity remaining in the genus Sphenodon extant tuatara into a single species, S. punctatus . and deserve special recognition and protection. Daugherty et al . (1990) reported allozyme and mor- However, recent results with other molecular tech- phological differences from 24 of the 30 islands on niques indicate that the tuatara on North Brother which tuatara are thought to remain. These studies Island probably do not warrant recognition as a dis- support the status of S. guntheri as a distinct species tinct species (Hay et al . 2010 , Example 16.3 ). On a larger taxonomic scale, how should we value the tuatara relative to other species of reptiles? Tuatara species are the last remaining representatives of the Sphenodontida, one of four extant orders of reptiles (tuatara, snakes and lizards, alligators and crocodiles, and tortoises and turtles). In contrast, there are approximately 5000 species in the Squa- mata, the speciose order that contains lizards and snakes. One position is that conservation priorities should regard all species as equally valuable. This position would equate the two tuatara species with any two species of reptiles. Another position is that we should take phylogenetic diversity into account in assigning conservation priorities. The extreme phylogenetic position is that we should assign equal conservation value to each major sister group in a phylogeny. According to this position, tuatara would be weighed equally with the over 5000 species of other snakes and lizards. Some intermediate between these two Figure 1.1 Adult male tuatara. positions seems most reasonable.

There is great appeal to placing conservation empha- Among the many primitive features of the tuatara is a sis on distinct evolutionary lineages with few living rudimentary third, or pineal, eye on the top of the relatives. Living fossils, such as the tuatara, ginkgo head. (Royer et al . 2003 ), or the coelacanth (Thompson Tuatara represent an important ancestral outgroup 1991 ), represent important pieces in the jigsaw puzzle for understanding vertebrate evolution. For example, a of evolution. Such species are relics that are represent- recent study has used genomic information from atives of taxonomic groups that once fl ourished. Study tuatara to reconstruct and understand the evolution of of the primitive morphology, physiology, and behavior 18 human retroposon elements (Lowe et al . 2010 ). of living fossils can be extremely important in under- Most of these elements were quickly inactivated early in standing evolution. For example, tuatara morphology the mammalian lineage, and thus study of other has hardly changed in nearly 150 million years. mammals provides little insight into these elements in Introduction 7 humans. These authors conclude that species with his- esis. In addition, species such as C, D, E, and F may be torically low population sizes (such as tuatara) are more widespread, and therefore are not likely to be the object likely to maintain ancient mobile elements for long of conservation efforts. periods of time with little change. Thus, these species The problem is more complex than just identifying are indispensable in understanding the evolutionary species with high conservation value; we must take a origin of functional elements in the human genome. broader view and consider the habitats and environ- In contrast, others have argued that our conserva- ments where our conservation efforts could be concen- tion strategies and priorities should be based primarily trated. Conservation emphasis on phylogenetically upon conserving the evolutionary process rather than distinct species will lead to protection of environments preserving only those pieces of the evolutionary puzzle that are not likely to contribute to future evolution that are of interest to humans (Erwin 1991 ). Those (e.g., small islands along the coast of New Zealand). In species that will be valued most highly under the contrast, geographic areas that are the center of evo- schemes that weigh phylogenetic distinctness are those lutionary activity for diverse taxonomic groups could that may be considered evolutionary failures. Evolu- be identifi ed and targeted for long - term protection. tion occurs by changes within a single evolutionary Recovery from our current extinction crisis should lineage ( anagenesis) and the branching of a single be a central concern of conservation (Myers et al . evolutionary lineage into multiple lineages (cladogen- 2000 ). It is important to maintain the potential for the esis ). Conservation of primitive, nonradiating taxa is generation of future biodiversity. We should identify not likely to be benefi cial to the protection of the evo- and protect contemporary hotspots of evolutionary lutionary process and the environmental systems that radiation and the functional taxonomic group from are likely to generate future evolutionary diversity which tomorrow’ s biodiversity is likely to originate. In (Erwin 1991 ). addition, we should protect those phylogenetically dis- Figure 1.2 illustrates the phylogenetic relations tinct species that are of special value for our under- among seven hypothetical species (from Erwin 1991 ). standing of biological diversity and the evolutionary Species A and B are phylogenetically distinct taxa that process. These species are also potentially valuable for are endemic to small geographic areas (e.g., tuataras future evolution of biodiversity because of their com- in New Zealand). Such lineages carry information bination of unusual phenotypic characteristics that about past evolutionary events, but they are relatively may give rise to a future evolutionary radiation. Isaac unlikely to be sources of future evolution. In contrast, et al . (2007) have proposed using an index that com- the stem resulting in species C, D, E, and F is relatively bines both evolutionary distinctiveness and IUCN Red likely to be a source of future anagenesis and cladogen- List categories to set conservation priorities.

Centers of endemism Evolutionary front Area 1 Area 2 Area 3 A B CDE F

Time

Figure 1.2 Hypothetical phylogeny of seven species. Redrawn from Erwin (1991) . 8 Introduction

1.2.2 Populations, s pecies, or e cosystems? Ceballos and Ehrlich (2002) have compared the his- torical and current distributions of 173 declining A related, and sometimes impassioned, dichotomy mammal species from throughout the world. Their between protecting centers of biodiversity or phyloge- data included all of the terrestrial mammals of Aus- netically distinct species is the dichotomy between tralia and subsets of terrestrial mammals from other emphasis on species conservation or on the conserva- continents. Nearly 75% of all species they included tion of habitat or ecosystems (Soulé and Mills 1992 , have lost over 50% of their total geographic range. Armsworth et al . 2007 ). Conservation efforts to date Approximately 22% of all Australian species are declin- have emphasized the concerns of individual species. ing, and they estimated that over 10% of all Australian For example, in the US the Endangered Species Act terrestrial mammal populations have been extirpated (ESA) has been the legal engine behind much of the since the 19th century. These estimates, however, all conservation efforts. However, it is frustrating to see assume that population extirpation is proportional to enormous resources being spent on a few high profi le loss of range area rather than defi ning populations species when little is spent on less charismatic taxa or using genetic criteria. in preventing environmental deterioration that would The amount of genetic variation within a popula- benefi t many species. It is clear that a more compre- tion may also play an important ecosystem role in the hensive and proactive conservation strategy emphasiz- relationships among species in some functional groups ing protection of habitat and ecosystems, rather than and ecosystems. Clark (2010) has found that intraspe- species, is needed. Some have advocated a shift from cifi c genetic variation within forest trees in the south- saving things, the products of evolution (species, com- eastern US allows higher species diversity. Recent munities, or ecosystems), to saving the underlying pro- results in community genetics suggest that individ- cesses of evolution “ that underlie a dynamic biodiversity ual alleles within some species can affect community at all levels” (Templeton et al . 2001 ). diversity and composition (Crutsinger et al . 2006 ). For It has been argued that more concern about extinc- example, alleles at tannin loci in cottonwood trees tion should be focused on the extinction of genetically affect palatability and decay rate of leaves, which in distinct populations, and less on the extinction of turn infl uences abundance of soil microbes, fungi, and species (Hughes et al. 1997 , Hobbs and Mooney 1998 ). arboreal insects and birds (Whitham et al . 2008 ). The conservation of many distinct populations is Genetic variation in the bark characteristics of a foun- required to maximize evolutionary potential of a dation species (Tasmanian blue gum tree) has been species and to minimize the long - term extinction risks found to affect the abundance and distribution of of a species. In addition, a population focus would also insects, birds, and marsupials. Loss or restoration of help to prevent costly and desperate ‘ last - minute ’ con- such alleles to populations could thus infl uence com- servation programs that occur when only one or two munity diversity and ecosystem function (Whitham small populations of a species remain. The fi rst attempt et al . 2008 ). to estimate the rate of population extinction worldwide Conservation requires a balanced approach that is was published by Hughes et al . (1997) . They estimated based upon habitat protection which also takes into that tens of millions of local populations that are genet- account the natural history and viability of individual ically distinct go extinct each year. Approximately 16 species. Consider Chinook salmon in the Snake River million of the world’ s three billion genetically distinct basin of Idaho, which are listed under the ESA. These natural populations go extinct each year in tropical fi sh spend their fi rst two years of life in small mountain forests alone. rivers and streams far from the ocean. They then Luck et al. (2003) have considered the effect of popu- migrate over 1500 km downstream through the Snake lation diversity on the functioning of ecosystems and and Columbia Rivers and enter the Pacifi c Ocean. There so - called ecosystem services. They argue that the they spend two or more years ranging as far north as relationship between biodiversity and human wellbe- the coast of Alaska before they return to spawn in their ing is primarily a function of the diversity of popula- natal freshwater streams. There is no single ecosystem tions within species. They have also proposed a new that encompasses these fi sh, other than the biosphere approach for describing population diversity that con- itself. Protection of this species requires a combination siders the value of groups of individuals to the services of habitat measures and management actions that that they provide. take into account the complex life - history of these fi sh. Introduction 9

1.3 HOW SHOULD WE CONSERVE the greater the probability of such effects. However, the BIODIVERSITY? effects of small population size are stochastic because we cannot predict what traits will be affected. Extinction is a demographic process: the failure of Under some conditions, extinction is likely to be one generation to replace itself with a subsequent gen- inﬂ uenced by genetic factors. Small populations are eration. Demography is of primary importance in man- also subject to genetic stochasticity, which can lead to aging populations for conservation (Lacy 1988 , Lande loss of genetic variation through genetic drift. The 1988 ). Populations are subject to uncontrollable sto- ‘ inbreeding effect of small populations ’ (see Box 1.1 ) is chastic demographic factors as they become smaller. It likely to lead to a reduction in the fecundity and viabil- is possible to estimate the expected mean and variance ity of individuals in small populations. For example, of a population ’ s time to extinction if one has an under- Frankel and Soulé (1981 , p. 68) suggested that a 10% standing of a population ’ s demography and environ- decrease in genetic variation due to the inbreeding ment (Goodman 1987 , Belovsky 1987 , Lande 1988 ). effect of small populations is likely to cause a 10– 25% There are two main types of threats causing extinc- reduction in reproductive performance of a population: deterministic and stochastic threats (Caugh- tion. This in turn is likely to cause a further reduction ley 1994 ). Deterministic threats are habitat destruction, in population size, and thereby reduce a population ’ s pollution, overexploitation, species translocation, and ability to persist (Gilpin and Soul é 1986 ). This has global climate change. Stochastic threats are random come to be known as the extinction vortex (see changes in genetic, demographic or environmental Figure 14.2 ). factors. Genetic stochasticity is random genetic change Some have argued that genetic concerns can be (drift) and increased inbreeding (Shaffer 1981 ). ignored when projecting the viability of small popula- Genetic stochasticity leads to loss of genetic variation tions because they are in much greater danger of (including beneﬁ cial alleles) and increase in frequency extinction by purely demographic stochastic effects of harmful alleles. An example of demographic sto- (Lande 1988 , Pimm et al . 1988 , Caughley 1994 , chasticity is random variation in sex ratios, for example Frankham 2003 , Sarre and Georges 2009 ). It has producing only male offspring. Environmental sto- been argued that such small populations are not likely chasticity is simply random environmental variation, to persist long enough to be affected by inbreeding such as the occasional occurrence of several harsh depression, and that efforts to reduce demographic winters in a row. In a sense, the effects of small popula- stochasticity will also reduce the loss of genetic variation size are both deterministic and stochastic. We tion. The disagreement over whether or not genetics know that genetic drift in small populations is likely to should be considered in demographic predictions of have harmful effects, and the smaller the population, population persistence has been unfortunate and

Box 1.1 What is an ‘ i nbred ’ p opulation?

The term ‘ inbred population’ is used in the literature individuals to mate with one another. For example, to mean two very different things (Chapter 13 , Tem- many extremely large populations of pine trees are pleton and Read 1994 ). In the conservation literature, inbred because of their spatial structure (see Section ‘ inbred population’ is often used to refer to a small 9.2 ). Nearby trees tend to be related to one another population in which mating between related individu- because of limited seed dispersal, and nearby trees als occurs because after a few generations, all indi- also tend to fertilize each other because of wind pol- viduals in a small population will be related. Thus, lination. Therefore, a population of pine trees with matings between related individuals (inbreeding) will millions of individuals may still be ‘ inbred’ . occur in small populations even if they are random Population genetics is a complex fi eld. The incor- mating (panmictic). This has been called the ‘ inbreed- rect, ambiguous, or careless use of words can some- ing effect of small populations’ (see Chapter 6 ). times result in unnecessary confusion. We have made Formally in population genetics, an ‘ inbred’ popula- an effort throughout this book to use words precisely tion is one in which there is a tendency for related and carefully. 10 Introduction misleading. Extinction is a demographic process that is of the populations involved (Lacy 2000b ). A similar likely to be infl uenced by genetic effects under some statement can be made about most of the issues we are circumstances. The important issue is to determine faced with in conservation biology. We can only resolve under what conditions genetic concerns are likely to these problems by an integrated approach that incor- infl uence population persistence (Nunney and Camp- porates demography and genetics, as well as other bio- bell 1993 ). logical considerations that are likely to be critical for a Perhaps most importantly, we need to recognize particular problem (e.g., behavior, physiology, inter- when management recommendations based upon specifi c interactions, as well as habitat loss and envi- demographic and genetic considerations may be in ronmental change). confl ict with each other. For example, small populations face a variety of genetic and demographic effects that threaten their existence. Management plans aim 1.4 APPLICATIONS OF GENETICS TO to increase the population size as soon as possible to CONSERVATION avoid the problems associated with small populations. However, efforts to maximize growth rate may actually Darwin (1896) was the fi rst to consider the importance increase the rate of loss of genetic variation by relying of genetics in the persistence of natural populations. on the exceptional reproductive success of a few indi- He expressed concern that deer in British nature parks viduals (see Example 19.1 , Caughley 1994 ). may be subject to loss of vigor because of their small Ryman and Laikre (1991) considered what they population size and isolation. Voipio (1950) presented termed supportive breeding in which a portion of the fi rst comprehensive consideration of the applica- wild parents are brought into captivity for reproduc- tion of population genetics to the management of tion and their offspring are released back into the natural populations. He was primarily concerned with natural habitat where they mix with wild conspecifi cs. the effects of genetic drift in game populations that Programs similar to this are carried out in a number of were reduced in size by trapping or hunting and frag- species to increase population size and thereby temper mented by habitat loss. stochastic demographic effects (e.g., Blanchet et al . The modern concern for genetics in conservation 2008 ). Under some circumstances, supportive breed- began around 1970 when Sir Otto Frankel (Frankel ing may reduce effective population size and cause a 1970 ) began to raise the alarm about the loss of primi- drastic reduction in genetic heterozygosity (Ryman tive crop varieties and their replacement by genetically 1994 ). uniform cultivars (see Guest Box 1 ). It is not surprising Genetic information also can provide valuable that these initial considerations of conservation genet- insight into the demographic structure and history of ics dealt with species that were used directly as a population (Escudero et al . 2003 ). Estimation of the resources by humans. Conserving the genetic resources number of unique genotypes can be used to estimate of wild relatives of agricultural species remains an total population size in populations that are diffi cult to important area of conservation genetics (Maxted census (Luikart et al . 2010 ). Many demographic 2003 , Hanotte et al . 2010 ). A surprisingly modern models assume a single random mating population. view of the importance and role of genetics in conser- Examination of the distribution of genetic variation vation was written by J.C. Greig in 1979 . This interest- over the distribution of a species can identify what geo- ing paper emphasized the importance of maintaining graphic units can be considered separate demographic the integrity of local population units. units. Consider the simple example of a population of The application of genetics to conservation in a trout found within a single small lake for which it more general context did not blossom until around would seem appropriate to consider these fi sh a single 1980 , when three books established the foundation for demographic unit. However, under some circum- applying the principles of genetics to conservation of stances the trout in a single small lake can actually biodiversity (Soulé and Wilcox 1980 , Frankel and represent two or more separate reproductive (and Soul é 1981 , Schonewald - Cox et al . 1983 ). Today demographic) groups with little or no exchange conservation genetics is a well- established discipline, between them (e.g., Ryman et al . 1979 ). with its own journals ( Conservation Genetics and Con- The issue of population persistence is a multidiscipli- servation Genetics Resources) and two textbooks, includ- nary problem that involves many aspects of the biology ing this one and Frankham et al . (2010) . Introduction 11

Maintenance of biodiversity primarily depends upon may lead to predictions of the relative susceptibility the protection of the environment and maintenance of of ecosystems to invasion, identifi cation of key alien habitat. Nevertheless, genetics has played an impor- species, and predictions of the subsequent effects of tant and diverse role in conservation biology in the last removal. few years. Nearly 10% of the articles published in the Recent advances in molecular genetics, including journal Conservation Biology since its inception in 1988 sequencing of the entire genomes of many species, have “ genetic ” or “ genetics ” in their title. Probably at have revolutionized applications of genetics (e.g., med- least as many other articles deal with largely genetic icine, forestry, and agriculture). For example, it has concerns but do not have the term in their title. Thus, been suggested that genetic engineering should be con- some 15% of the articles published in Conservation sidered as a conservation genetics technique (Adams Biology have genetics as a major focus. et al. 2002 ). Many native trees in the northern temper- The subject matter of papers published on conserva- ate zone have been devastated by introduced diseases tion genetics is extremely broad. However, most of arti- for which little or no genetic resistance exists (e.g., cles dealing with conservation and genetics fi t into one European and North American elms, and the North of the fi ve broad categories below: American chestnut. Adams et al . (2002) suggested 1 Management and reintroduction of captive popula- that transfer of resistance genes by genetic modifi ca- tions, and the restoration of biological communities. tion is perhaps the only available method for prevent- 2 Description and identifi cation of individuals, genetic ing the loss of important tree species. Transgenic trees population structure, kin relationships, and taxo- have been developed for both American elm and Amer- nomic relationships. ican chestnut, and are now being tested for stable 3 Detection and prediction of the effects of habitat resistance to Dutch elm disease and chestnut blight loss, fragmentation, and isolation. (Newhouse et al . 2007 ). The use of genetic engineering 4 Detection and prediction of the effects of hybridiza- to improve crop plants has been very controversial. tion and introgression. There no doubt will continue to be a lively debate in the 5 Understanding the relationships between adapta- near future about the use of these procedures to tion or fi tness and genetic characters of individuals prevent the extinction of natural populations. or populations. The loss of key tree species is likely to affect many These topics are listed in order of increasing complex- other species as well. For example, whitebark pine is ity and decreasing uniformity of agreement among currently one of the two most important food resources conservation geneticists. Although the appropriate- for grizzly bears in the Yellowstone National Park eco- ness of captive breeding in conservation has been con- system (Mattson and Merrill 2002 ). However, virtually troversial (Snyder et al. 1996 , Adamski and Witkowski all of the whitebark pine in this region is projected to 2007 , Fraser 2008 ), procedures for genetic manage- be extirpated because of an exotic pathogen (Mattson ment of captive populations are well developed with et al. 2001 ), and with predicted geographic shifts in the relatively little controversy. However, the relationship climatic niche - based habitat of this species in the next between specifi c genetic types and fi tness or adaptation century (Warwell et al . 2007 ). has been a particularly vexing issue in evolutionary There are a variety of efforts around the world to and conservation genetics. Nevertheless, studies have store samples of DNA libraries, frozen cells, gametes, shown that natural selection can bring about rapid and seeds that could yield DNA (Frozen Ark Project, genetic changes in populations that may have impor- Millennium Seed Bank Project, Svalbard Global Seed tant implications for conservation (Stockwell et al . Vault, Ryder et al . 2000 ). The hope is that these 2003 ). resources would at least provide complete genome Invasive species are recognized as one of the top two sequences of species that might become extinct in the threats to global biodiversity (Chapter 20 ). Studies of not- distant future. These sequences could be invalua- genetic diversity and the potential for rapid evolution ble for reconstructing evolutionary relationships, of invasive species may provide useful insights into understanding how specifi c genes arose to encode what causes species to become invasive (Lee and proteins that perform specialized functions, and how Gelembiuk 2008 ). More information about the genet- the regulation of genes has evolved. In some cases (e.g., ics and evolution of invasive species or native species seed banks), these resources could be used to recover in invaded communities, as well as their interactions, apparent extinct species. 12 Introduction

1.5 THE FUTURE make it possible to answer many important questions in conservation that have been intractable until now Genetics is likely to play even a greater role in conser- (Figure 1.3 ). vation biology in the future (Primmer 2009 , Ouborg As in other areas of genetics, model organisms have et al . 2010 , Avise 2010 , Frankham 2010 ). We will played an important research role in conservation soon have complete genome sequences from thou- genetics (Frankham 1999 ). Many important theoreti- sands of species, as well as many individuals within cal issues in conservation biology cannot be answered species (Haussler et al . 2009 ). This coming explosion by research on threatened species (e.g., how much of information will transform our understanding of gene fl ow is required to prevent the inbreeding effects the amount, distribution, and functional signifi cance of small population size?). Such empirical questions of genetic variation in natural populations (Amato are often best resolved in species that can be raised in et al . 2009 , Allendorf et al. 2010 ). Now is a crucial time captivity in large numbers with a rapid generation to explore the potential implications of this informa- interval (e.g., the fruit fl y Drosophila , the guppy, deer tion revolution for conservation genetics, as well as to mouse, and the fruit - fl y equivalent in plants, Arabidop- recognize limitations in applying genomic tools to con- sis ). The genome sequencing of plant and animal servation issues. The ability to examine hundreds or model and agricultural species have been crucial for thousands of genetic markers with relative ease will transferring genomic tools to wild populations of other

Population size Population structure

Migration rates

Genetic drift Inbreeding Hybridization

Loss of genetic Genotype-by-environment Local diversity interactions adaptation

Loss of adaptive Inbreeding Outbreeding variation depression depression

Demographic vital rates

Population growth or viability

Figure 1.3 Schematic diagram of interacting factors in the conservation of natural populations. Traditional conservation genetics, using neutral markers, provides direct estimates of some of these factors (outlined by solid lines). Conservation genomics can address a wider range of factors (outlined by dashed lines). It also promises more precise estimates of neutral processes and understanding of the specifi c genetic basis of all of these factors. For instance, traditional conservation genetics can estimate overall migration rates or inbreeding coeffi cients, while genomic tools can assess gene fl ow rates specifi c to adaptive loci or founder- specifi c inbreeding coeffi cients. From Allendorf et al . (2010) . Introduction 13 species. Such laboratory investigations can also provide in the laboratory (Wayne and Morin 2004 , Allendorf excellent training opportunities for students. We have et al . 2010 ). However, interpretation of this explosion tried to provide a balance of examples from model and of data requires a solid understanding of population threatened species. Nevertheless, where possible we genetics theory (see Preface, Figure i.1 ). This book is have chosen examples from threatened species, even meant to provide a thorough examination of our though many of the principles were fi rst demonstrated understanding of the genetic variation in natural pop- with model species. ulations. Based upon that foundation, we will consider This is an exciting time to be interested in the genet- the application of this understanding to the many ics of natural populations. Molecular techniques make problems faced by conservation biologists, with the it possible to detect genetic variation in any species of hope that our more informed actions can make a interest, not just those that can be bred and studied difference.

Guest Box 1 The r ole of g enetics in c onservation L. Scott Mills and Michael E. Soul é

Until recently, most conservationists ignored genet- in the late 1980s and early 1990s argued that – ics and most geneticists ignored the biodiversity compared with demographic and environmental catastrophe. It was agricultural geneticists, led by accidents – inbreeding and loss of genetic variation Sir Otto Frankel (1974) , who began to sound an were trivial contributors to extinction risk in small alarm about the disappearance of thousands of populations. Eventually, however, this swing in sci- land races – crop varieties coaxed over thousands entiﬁ c fashion was arrested by the friction of real of years to adapt to local soils, climates, and pests. world complexity.

Frankel challenged geneticists to help promote an Thanks to the work of F 1 and F 2 conservation “ evolutionary ethic ” focused on maintaining evolu- geneticists, it is now clear that inbreeding depres- tionary potential and food security in a rapidly sion can increase population vulnerability by inter- changing world. acting with random environmental variation, not Frankel ’ s pioneering thought inspired the fi rst to mention deterministic factors including habitat international conference on conservation biology degradation, new diseases, and invasive exotics. in 1978. It brought together ecologists and evolu- Like virtually all dualisms, the genetic versus non- tionary geneticists to consider how their fi elds could genetic battles abated in the face of the overwhelm- help slow the extinction crisis. Some of the chapters ing evidence for the relevance of both. in the proceedings (Soul é and Wilcox 1980 ) fore- Genetic approaches have become prominent in shadowed population viability analysis and the other areas of conservation biology as well. These interactions of demography and genetics in small include: (1) the use of genetic markers in forensic populations (the extinction vortex). Several subse- investigations concerned with wildlife and endan- quent books (Frankel and Soulé 1981 , Schonewald- gered species; (2) genetic analyses of hybridization Cox et al . 1983 , Soul é 1987a ) consolidated the role and invasive species; (3) noninvasive genetic esti- of genetic thinking in nature conservation. mation of population size and connectivity; and (4) Thus, topics such as inbreeding depression and studies of taxonomic affi liation and distance. And, loss of heterozygosity were prominent since the of course, the overwhelming evidence of rapid beginning of the modern discipline of conservation climate change has renewed interest in the genetic biology, but like inbred relatives, they were conven- basis for adaptation as presaged by Frankel 30 years iently forgotten at the end of the 20th century. ago. Nowadays, genetics is an equal partner with Why? Fashion. Following the human proclivity to ecology, systematics, physiology, epidemiology, and champion simple, singular solutions to complex behavior in conservation, and both conservation problems, a series of papers on population viability and genetics are enriched by this pluralism.