www.esf.org

INTEGRATING POPULATION GENETICS AND CONSERVATIONBIOLOGY: MERGING THEORETICAL, EXPERIMENTAL ANDAPPLIED APPROACHES (ConGen)Standing Committee for Life,Earth and Environmental Sciences (LESC)

RESEARCH NETWORKING PROGRAMME

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The European Science Foundation (ESF) was established in 1974 to create a common European platform forcross-border cooperation in all aspects of scientific research.

With its emphasis on a multidisciplinary and pan-European approach, the Foundation provides the leadershipnecessary to open new frontiers in European science.

Its activities include providing science policy advice (Science Strategy); stimulating cooperation betweenresearchers and organisations to explore new directions (Science Synergy); and the administration of externallyfunded programmes (Science Management). These take place in the following areas: Physical and engineeringsciences; Medical sciences; Life, earth and environmental sciences; Humanities; Social sciences; Polar;Marine; Space; Radio astronomy frequencies; Nuclear physics.

Headquartered in Strasbourg with offices in Brussels, the ESF’s membership comprises 75 national fundingagencies, research-performing agencies and academies from 30 European nations.

The Foundation’s independence allows the ESF to objectively represent the priorities of all these members.

Cover picture : The Florida panther (bottom left, photo courtesy US Fish and Wildlife Services, see also figure 3), the beaver (top left, see also figure 3), the Bezoar goat (top right, photo courtesyOsman Yöntem) and the Siberian Jay (bottom right, photo courtesy Hannu Siitonen) are all speciesthat have suffered from human impact on nature and as such have become endangered. For instance, the Bezoar goat (wild goat, Capra aegagrus aegagrus), here pictured in TermessosNational Park (Turkey), is classified by the IUCN as vulnerable as numbers are decreasing mainlybecause of hunting. The Siberian jay (Perisoreus infaustus) is a species which has suffered particularlyfrom the loss and fragmentation of the boreal coniferous forests. At least some of the populations of this species have become highly inbred.

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Human impact on nature has increased extinctionrates of populations and species dramatically andmany species are currently on the brink ofextinction. Habitat deterioration, fragmentation anddestruction are now recognised as a major threat tothe persistence of populations and species. Withinthe field of conservation biology the role ofconservation genetics has been greatlyemphasised. This role is twofold. On the one hand,conservation genetics provides the tools to studythe demographic dynamics of endangered species(e.g. by the use of molecular genetic markers), toinfer their past history (identification of bottlenecksand population expansions), to resolve taxonomicuncertainties, and to define management units. Onthe other hand it studies the consequences ofgenetic processes that are inevitable in smallfragmented populations: genetic drift andinbreeding will cause loss of genetic diversity andan increase in homozygosity. This process ofgenetic erosion can seriously reduce the adaptivepotential of populations to changing anddeteriorating environments, can decrease averageindividual fitness (inbreeding depression) and,consequently, can significantly increase theextinction risk of endangered species.

The emerging field of conservation genetics cansignificantly contribute to the preservation of nature.Different approaches and methodologies, i.e.theoretical, experimental and applied, are neededto build a consistent framework. The ESF ResearchNetworking Programme on Integrating PopulationGenetics and Conservation Biology: MergingTheoretical, Experimental and Applied Approaches(ConGen) aims at providing a venue for concertedscientific action in the field of conservation genetics,and to combine and integrate the differentperspectives.

The running period of the ConGen Programme isfor five years, from November 2004 to November2009.

Introduction

Fig. 1: Genetic studies also have an importantrole in re-introduction and supplementation programmes

of wild populations with captive stocks.Studies of captive stocks of the Lesser white-fronted goose

(Anser erythropus) have revealed several hybridisationevents with other geese species, making captive

stocks unsuitable for re-introductions. (Photo courtesy Ingar Jostein Øien)

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Human impact on nature

Many plant and animal species currently have to copewith human-induced alterations of their naturalenvironment. Climate is changing globally at a speedthat is higher than has been observed in the past 10 000 years and projections into the future show anacceleration of global temperature rise. Chemicalpollution and other alterations in the physical habitathave caused the environment to become more andmore hostile. In addition, destruction of naturalhabitats for agricultural development, industrialisationand urbanisation have caused – and still cause – aconsiderable decline in population numbers and anincrease in extinction. Importantly, suitable habitat notonly deteriorates but also becomes greatlyfragmented, leaving isolated patches of habitat in anotherwise uninhabitable ’desert’. This will certainlyimpede migration rates and lead to decreasedconnectivity between populations. Consequently,many (endangered) species find themselves confinedto small habitat patches that can sustain only a limitednumber of individuals. As such, these smallpopulations become increasingly affected bystochastic events, which significantly increase theprobability of extinction through randomdemographic, environmental and genetic forces. It isestimated that a significant proportion of the world’sspecies may become extinct in the next few decades,while many more species are considered to be eitherendangered or vulnerable to extinction.

Genetics and conservation biology

Conservation biology is the scientific discipline thatdeals with understanding the forces involved inbiodiversity dynamics and provides principles andtools for preserving biodiversity. Within this fieldconservation genetics deals with (i) the geneticprocesses that affect the persistence of populationsand species, of which genetic erosion is central, andincludes development of management measures forminimising the extinction risks related to geneticerosion; (ii) genetics also provides the tools todescribe the structure and dynamics of biodiversity atthe genetic level, both in the past and at present, andit also provides the tools to study and to inferevolutionary change; and (iii) genetics provides thetools to determine important aspects of the biology ofendangered species and to estimate importantecological parameters, e.g. factors concerning thereproductive system of a species, dispersal andmigrations patterns. Such data are often crucial todevising adequate management measures. Althoughin the past there has been some discussion about therelative importance of ecological and geneticprocesses in relation to the extinction risk ofendangered species, it is now well established thatthese should be studied in concert becausegenotype-by-environment interaction affect both.

Integrating all these aspects, tools and processes willcontribute importantly to understanding theconsequences of changing and stressfulenvironments, habitat fragmentation andaccompanying genetic erosion for extinction risksand the dynamics of adaptation of species to human-induced alterations of the natural environment,forming the new scientific discipline of conservationgenetics.

Background

The founding ideas of conservation genetics in the1980s concerned the impact of genetic drift andinbreeding on population persistence. Though theissue of genetic erosion has remained central, thefield has since then greatly expanded. Broadlyspeaking, the scientific research currently focuseson two interrelated topics. First, research into theimpact of genetic erosion on mean fitness and theextinction risks of endangered species, particularlyin relation to changing and deterioratingenvironments. Second, the value and use ofdifferent molecular markers and other tools incharacterising (adaptive) diversity, analysing thedemographic structure and dynamics ofendangered populations, and inferring conservationunits. In the end, conservation genetics should beaimed at providing information, tools and guidelinesfor (genetic) management of small, endangeredpopulations and species. Several important issuesthat dominate the field of conservation genetics arehighlighted below.

Inbreeding depression and extinction

Genetic erosion in small isolated populations isthought to result in an increase in homozygositywhereby recessive deleterious alleles becomeexpressed causing a decrease of fitness:inbreeding depression. There is little doubt thatinbreeding depression can be severe in normallyoutcrossing species. However, except for somelaboratory experiments, it is still difficult to show thedirect effects of inbreeding depression onpersistence, particularly for natural conditions. Forone thing, this may be because the effects undernormal conditions are subtle and accumulate slowlyand thus may become apparent only in the longterm. For another thing, genetic and ecologicalfactors are not independent and are often difficult todisentangle.

Therefore, studies that integrate genetic,environmental and demographic processes areneeded. This is the more important because severalobservations suggest that the consequences ofgenetic erosion become more pronounced understress conditions, thereby greatly increasingmortality and extinction probabilities. Thissynergistic interaction between inbreedingdepression and environmental stress is currentlypoorly understood and based on limited studies.Thus there is a great need to increase and extendthose studies also to natural conditions.

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Scope of the Programme

Fig. 2: The problems of genetic erosion can be experimentallyinvestigated using Drosophila as the model organism.

The figures show the percentage extinction of smallDrosophila populations (30-100 individuals) in relation

to the degree of inbreeding (F-value) these populationshad experienced prior to the experiment.

The experiment was done under benign conditions (top)and stress, high temperature, conditions (bottom).

Clearly, the extinction risk of small populations increaseswhen the level of genetic erosion increases. Importantly,

this effect is strongly amplified under stressful conditions.(After Bijlsma et al. (2000) J. Evol. Biol. 13:502).

generations

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Purging and the geneticarchitecture of inbreeding depression

When genetically eroded, there is also considerablevariation in the magnitude of inbreeding depression,not only for different life history traits, but alsobetween species. Upon inbreeding, some speciesseem to suffer greatly from inbreeding depressionwhile others seemingly are unaffected by geneticerosion. In part, this might be due to the fact thatspecies have different life histories and differ indemographic parameters. For another part, it hasbeen suggested that a sufficiently slow rate ofinbreeding may enable natural selection to purgedeleterious alleles from populations, therebyreducing the impact of inbreeding depression.Much also depends on the genetic architectureunderlying inbreeding depression, whether it iscaused by a few genes with large or many with asmall effect on fitness, by recessive oroverdominant alleles, or by epistatic and pleiotropiceffects. If we want to predict which species underwhat conditions will be impacted by inbreedingdepression, we need to know much more aboutthe causation of this phenomenon, its timing andhow this affects the possibility of purging.

Genetic rescue and outbreeding depression

Migration or gene flow between isolatedpopulations, either naturally or artificially by meansof translocation of individuals, may counteractinbreeding depression. This process of 'geneticrescue', however, is not without danger as differentpopulations may be locally adapted to differentenvironmental conditions. Imposing gene flow willthen lead to 'hybrids' that are not locally adaptedand consequently suffer from outbreedingdepression, thereby endangering the persistence ofthe threatened population even more. It is thereforeimportant to reliably assess the contribution ofoutcrossing depression to the extinction risk ofpopulations. Information about the degree andscale of local adaptation in metapopulations istherefore a prerequisite.

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Fig. 3: Contrasting examples of genetically eroded speciesthat differ greatly in their effects. The Florida panther

(Felis concolor coryi, top, photo courtesy US Fish andWildlife Services) population in the Everglades is highly

endangered as it has been small for a long timeand consequently shows many signs of inbreeding depression

(e.g. greatly decreased sterility).

The beaver (Castor fiber, bottom) population in Sweden hasgone through a severe bottleneck and is based on the level of

highly inbred genetic variation. Nevertheless, the populationhas greatly expanded from less than 50 around 1900 to more

than 100 000 currently, indicating that the population showsfew problems with inbreeding depression.

Environmental change and adaptive potential

Environmental stress is not only important inrelation to its impact on inbreeding depression, butalso imposes severe selection. As migration to amore optimal habitat is often not an option due tofragmentation, populations are forced to adapt,either phenotypically or genetically, to the changingenvironmental conditions. The rate and degree ofadaptation strongly depends on the amount andnature of standing genetic variation in a population.Since genetically eroded populations are expectedto have lower levels of variation, the adaptivepotential may have become greatly limited and thusthe extinction risk is increased. As, in contrast toneutral variation, little yet is known on the level,dynamics and nature of adaptive variation in smallpopulations; we need much more information tothis end. At the same time we need also to knowmuch more about the role and importance ofphenotypic plasticity in this respect.

Genetic markers: neutral versus selectedmarkers

An array of molecular genetic tools are currentlyavailable to investigate important characteristics ofpopulations. Neutral genetic markers, such asmicrosatellites, are widely used to assessinbreeding levels, the level of genetic variation,population structure, the connectivity betweenpopulations (gene flow), demographic parametersand phylogenetic or conservation units. In addition,assessment of neutral genetic variation is alsoinformative for inferring ancient or recent historicaldynamics of populations. Such data are vital forproviding practical solutions, resulting in tools andguidelines for management of endangered species.

However, such neutral data present limitations tomeasuring variation at loci that are related to fitnessand adaptation. Comparing differentiation betweenpopulations for neutral markers (Fst) to differentiationfor fitness-related traits (Qst) may partly mediate thisproblem. However, the latter measure is alsoaffected by the environmental conditions and maynot well reflect genetic differences. Therefore,development of non-neutral marker systems, e.g.SNPs in functional genes, and implementation ofmodern genomics techniques to study thedynamics of functional genes, to study adaptiveprocesses and to distinguish the consequences ofnatural selection from that of genetic drift, is ofutmost importance.

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Fig. 4: Illustration of the use of genetic markersfor assessing genetic variation within species.

The figure shows the variation at three microsatellite loci(marked green, blue and yellow, respectively;

the red bands are the result of a distance marker for referencepurposes) in a pine marten (Martes martes) population.

Each vertical lane shows the microsatellitepattern of a single individual. Clearly, all threemarkers are highly variable in this population.

Fig. 5: The pine marten (Martes martes) isan endangered species with a highly fragmented

population structure in many European countries.

Its genetic structure is currently analysed in order to evaluateits genetic status, to estimate connectivity between

(local) populations, and to asses phylogenetic relationships.Photo courtesy Aksel Bo Madsen.

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Theory: modelling approaches and softwaredevelopment

Conceptually, conservation genetics is soundlybased on existing population genetic and populationecology theory. However, this ‘classical’ evolutionaryframework was mainly constructed for reasonablylarge population and equilibrium situations.Unfortunately, in conservation genetics we aredealing with small populations fluctuating greatly insize, where the dynamics is highly stochastic andnon-equilibrium situations are the rule rather than theexception: metapoplations in which local populationscontinuously go extinct and become recolonised willprobably never attain an equilibrium situation.Moreover, the complexity and the many interactingprocesses involved cause convergence to acomparable genetic architecture of populations intime, even though the underlying demographic andgenetic processes differ fundamentally.

Consequently, there is a great need to extend andadapt existing theory and to develop new theoreticalmodels that will be tailored to such a highly dynamicsituation. To this end, individually based simulationmodels show great promise in combining geneticand ecological theory and may revolutioniseconservation genetic theory. Such models have to beevaluated and validated for their biological relevancein experiments using model organisms and ultimatelyhave to be validated in a natural setting. In addition,also the development of new software that combinesnew estimation and decision procedures integratinggenetic ecological and environmental data is crucial.

Scope of the Programme

Fig. 6: Example of the use of computer software to analyse thepopulation structure and migration patterns of endangered

species using multilocus microsatellite fingerprinting wherebyindividuals are clustered according to their genotypes. The topfigure shows the result for three samples from different badger

(Meles meles) populations in Denmark coloured according to theirsample location (DK-1: blue; DK-2: red; DK-3: green).

The individuals of the three populations in the majority areassigned to different clusters in the corners of the triangle,

indicating genetic differentiation between populations. However,some individuals sampled in one population cluster geneticallywith another population (blue individuals in the bottom corners)

and can be regarded as migrants from DK-1. Individuals along theside of the triangles can be interpreted as offspring of migrants

that share genetic information of two populations.

The bottom figure shows the result of the same exercise forsamples of two Dutch badger populations (marked blue and red,

respectively) combined with Danish badgers (marked green). Inthis case the Danish badgers cluster in the top corner, while theDutch individuals all are located along the basis of the triangle.

This indicates that Dutch and Danish badgers are clearlydifferentiated and totally isolated, whereas the two clusterspostulated within the Netherlands seem well connected by

migration. (Data Van de Zande et al (2007) J. Zool., in press).

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All the problems mentioned above are stronglyinterrelated and necessarily have to be approachedfrom different perspectives, requiring concertedaction of the different sub-disciplines in conservationgenetics. As such, the Programme on ConservationGenetics (ConGen) aims to promote:

(i) the development of theoretical models that willstrengthen the conceptual basis of conservationgenetics and allow better and more rigorouspredictions and provide a framework for designingcritical experiments, for decisively analysing empiricaldata, and for reliably developing guidelines formanagement.

(ii) the design and execution of critical experiments,both in the laboratory and under natural conditions,that, on the one hand, evaluate and test thepredictions from theory in a biological context andparameterise predictive models, on the other hand,disentangle and deconfound the effects of thedifferent underlying processes and causes involved.

(iii) the translation of the insights gained by theconceptual and experimental approaches intoschemes, tools and guidelines for the natural andapplied situation to provide practical solutions for themanagement of small endangered populations.

Integration of experimental, theoretical and appliedconservation genetics will certainly have strongsynergistic effects and will contribute significantly toimproving our understanding of methodological andapplied aspects of conservation genetics. In this way,we not only may come to a better understanding ofthreats that await biodiversity, but it will also allow usto devise better (management) measures toovercome the problems. ConGen will provide anexcellent platform for this.

The central objective of the Programme onConservation Genetics is to combine and integratethe different research areas involved in the field and tomerge European efforts and expertise to reach acritical mass of teams to lead the field worldwide. Thesynergy resulting from such an integration of scientificknowledge, methodological toolboxes and data willnot only lead to better insights into conservationgenetic issues but also provide crucial information forEuropean policies on conservation of biodiversity,e.g. in relation to global change and European-widenature conservation efforts. Many of the questionsaddressed in ConGen are questions currentlyaddressed in general evolutionary biology. Therefore,the merit of the programme is not restricted toconservation genetics but is also expected togenerate important scientific spin-off relevant for thewhole field of evolutionary biology.

Aims and Objectives

During its five year running period the programmewill:

a) educate and train young scientist ininterdisciplinary and collaborative research inthe complex field of conservation genetics;

b) review and standardise research approachesand evaluation procedures across Europe;

c) facilitate the implementation and developmentof new and recent molecular and theoreticaltools;

d) detect and evaluate new developments in thefield of conservation genetics and effectivelydisseminate the implications to the Europeanscientific community and make theseaccessible to other social actors such as naturemanagers and policy makers;

e) to establish a scientific network facilitatingaccess to, and exchange of, sample material ofendangered species across Europe.

These objectives will be pursued by carrying onthe following activities:

1) Training (courses and exchange visits)2) Workshop and conference organisation3) Communication and interactions with other

programmes

Programme Activities

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ESF Research Networking Programmes are principally funded by the Foundation’s Member Organisations onan à la carte basis. ConGen is supported by:

• Fonds zur Förderung der wissenschaftlichen Forschung (FWF)Austrian Science Fund, Austria

• Fonds voor Wetenschappelijk Onderzoek (FWO)Fund for Scientific Research – Flanders, Belgium

• Hrvatska akademija znanosti i umjetnosti (HAZU)Croatian Academy of Sciences and Arts, Croatia

• Akademie ved České republiky (AVČR)Academy of Sciences of the Czech Republic, Czech Republic

• Grantová agentura České republiky (GAČR)Grant Agency of the Czech Republic, Czech Republic

• Forskningsrådet for Natur og Univers (FNU)Natural Science Research Council, Denmark

• Finlands Akademi (AKA)Academy of Finland, Finland

• Centre National de la Recherche Scientifique (CNRS)National Centre for Scientific Research, France

• Országos Tudományos Kutatási Alapprogrammok (OTKA) Hungarian Scientific Research Fund, Hungary

• Magyar Tudomanyos Akademia (MTA)Hungarian Academy of Sciences, Hungary

• Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)Netherlands Organisation for Scientific Research, Netherlands

• Norges Forskningsråd (NFR)Research Council of Norway, Norway

• Comisión Interministerial de Ciencia y Tecnología (CICYT)Interministerial Committee on Science and Technology, Spain

• Consejo Superior de Investigaciones Científicas (CSIC)Council for Scientific Research, Spain

• Vetenskapsrådet (VR)Swedish Research Council, Sweden

• Türkiye Bilimsel ve Teknolojik ArastIrma Kurumu (TÜBITAK)Scientific and Technological Research Council of Turkey, Turkey

Funding

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Kuke Bijlsma (Chair)Centre of Ecological and EvolutionaryStudiesUniversity of GroningenKerklaan 309751 NN Haren NetherlandsTel: +31 50 363 2117Fax: +31 50 363 2348 Email: r.bijlsma@biol.rug.nl

Volker Loeschcke (Co-Chair)Department of Ecology and GeneticsInstitute of Biological SciencesUniversity of AaarhusNy Munkegade - Bygning 5408000 Aarhus CDenmarkTel: +45 89 42 32 68Fax: +45 86 12 71 91 Email: volker.loeschcke@biology.au.dk

Krunoslav Brcic-KosticDepartment of Molecular GeneticsRudjer Boskovic InstituteBijenicka 5410000 Zagreb CroatiaTel: +385 1 456 11 11Fax: +385 1 456 11 77Email: brcic@irb.hr

Josef BryjaInstitute of Vertebrate BiologyAcademy of Sciences of the CzechRepublicKvetná 8603 65 Brno Czech RepublicTel: +420 543 422 500Fax: +420 568627950Email: bryja@brno.cas.cz

Reinhard BürgerInstitut für MathematikUniversität WienNordbergstrasse 15, UZA41090 Vienna AustriaTel: +43 1 4277 506 31Fax: +43 1 4277 506 50 Email: Reinhard.Buerger@univie.ac.at

Battal CiplakDepartment of BiologyFaculty of Art and ScienceAkdenis UniversityArapsuyu07058 Antalya TurkeyTel: +90 242 310 2356Fax: +90 242 227 8911 Email: ciplak@akdenis.edu.tr

Luc De MeesterLaboratory of Aquatic EcologyKatholieke Universiteit LeuvenCh. De Bériotstraat 323000 Leuven BelgiumTel: +32 16 32 37 08Fax: +32 16 32 45 75 Email: luc.demeester@bio.leuven.be

Kjetil HindarNorwegian Institute of NatureResearchTungasletta 27485 Trondheim NorwayTel: +47 73 80 15 46Fax: +47 73 80 14 01Email: kjetil.hindar@nina.no

Martin LascouxDept of Evolutionary FunctionalGenomicsUppsala UniversityNorbyvagen 18D752 36 UppsalaSwedenTel: +46 18 471 64 16Fax: +46 18 471 64 24Email: Martin.Lascoux@ebc.uu.se

Juha MeriläDepartment of Population BiologyUniversity of HelsinkiPO Box 6500014 University of Helsinki FinlandTel: +358 40 837 4165Fax: +358 9 1915 7694 Email: juha.merila@helsinki.fi

Isabelle OlivieriUMR 5554Institut des Sciences de l'EvolutionUniversité Montpellier IIPlace Eugène Bataillon34095 Montpellier Cedex 05FranceTel: +33 4 67 14 37 50Fax: +33 4 67 14 37 22Email: olivieri@isem.univ-montp2.fr

Miguel TejedoCSICEstación Biológica de DoñanaAvenida Maria Luisa s/n, Pabellon delPerú41013 SevillaSpainEmail: tejedo@ebd.csic.es

Varga ZoltánDepartment of Zoology and EvolutionDebrecen UniversityEgyetem tér 14032 DebrecenHungaryTel: +36 52 512 900/2331Fax: +36 52 512 941Email: zvarga@tigris.unideb.hu

Coordination and ConGenwebmasterCino Pertoldi Department of Ecology and GeneticsInstitute of Biological SciencesUniversity of AaarhusNy Munkegade - Bygning 5408000 Aarhus CDenmarkTel: +45 8612 7191Email: cino.pertoldi@biology.au.dk

ESF Liaison

Astrid LunkesScience

Céline SeewaldAdministration

Life, Earth and EnvironmentalSciences Unit (LESC)European Science Foundation 1 quai Lezay-Marnésia BP 90015 67080 Strasbourg cedex FranceTel: +33 (0)3 88 76 71 58Fax: +33 (0)3 88 37 05 32Email: cseewald@esf.org

For the latest information on thisResearch Networking Programmeconsult the ConGen websites:www.esf.org/congenwww.congen.biz

ConGen Steering Committee

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