Local adaptation vs inbreeding depression in marginal populations of a Mediterranean alpine plant

Local adaptation versus inbreeding depression in marginal populations of a Mediterranean alpine plant: are they worthy

of conservation in a context of climate change?

Morente-López, J., García-Fernández, A., Lara-Romero, C., Rubio-Teso, M.L., Ruiz, R., Sánchez, A., Iriondo, J.M.

Área de Biodiversidad y Conservación, Universidad Rey Juan Carlos, E-28933 Móstoles, Madrid, Spain.

• Genetically impoverished populations

• Inbreeding depression• Maladaptation

• Not necessarilydepauperate for variationin ecologically relevanttraits.

• Locally adapted

Introduction Aims Materials & Methods Results & Discussion Conclusions

Marginal populations:• grow under suboptimal environmental conditions• great fluctuations and high probability of extinction

Soulé (1973)

?

Kawecki, T. J. 2008. Annu. Rev. Ecol. Evol. Syst. 39:321–342.

Soulé M. 1973. Annu. Rev. Ecol. Sys. 4:165-187

Lande R. 1994. Evolution 48: 1460–1469.

Whitlock MC. 2003. Genetics 164: 767–779.

Lande (1994), Whitlock (2003) Kawecki (2008)

Mediterranean alpine environments: highly vulnerable to global warming

Introduction Aims Materials & Methods Results & Discussion Conclusions

Marginal populations

Central populations

temperature rainfall

Experimental gene flow between populations:• assessment of inbreeding depression and geneflow of

adaptive/maladaptive value

• management tool to assist marginal populations

Introduction Aims Materials & Methods Results & Discussion Conclusions

Marginal populations

Central populations

central – marginal geneflow:• Genetic diversity (Holt & Gomulkiewicz, 1997)• Maladaptive alleles or gene combinations

(Kirkpatrick & Barton, 1997)

Holt RD, Gomulkiewicz R. 1997. Am Nat 149:563-572Kirkpatrick M, Barton NH. 1997. Am Nat 150:1-23

Experimental gene flow between populations:• assessment of inbreeding depression and geneflow of

adaptive/maladaptive value

• management tool to assist marginal populations

Introduction Aims Materials & Methods Results & Discussion Conclusions

Marginal populations

Central populations

marginal-marginal geneflow• Genetic diversity & adaptive alleles or gene combinations (Sexton et al. 2011)

Sexton JP, Strauss SY, Rice KJ. 2011. PNAS 108:11704-11709

Aim:

• To assess whether marginal populations at the lowest elevation of Mediterranean alpine plants are locally adapted/maladapted to the environmental conditions that will prevail with global warming

Introduction Aims Materials & Methods Results & Discussion Conclusions

• Circum-mediterranean alpine chamaephyte

• Central System at the lowest latitude of the distibution range:• Sierra de Béjar• Sierra de Gredos• Sierra de Guadarrama

• Elevation range: 1900 – 2500 m

Introduction Aims Materials & Methods Results & Discussion Conclusions

Silene ciliata Pourret

Introduction Aims Materials & Methods Results & Discussion Conclusions

• Central population

• Marginal populations

GuadarramaGredosBéjar

Central vs. marginal populations

(Giménez-Benavides et al. 2011)

Giménez-Benavides, L., Albert, M.J., Iriondo, J.M. & Escudero, A. Ecography (2011) 34:85-93

Introduction Aims Materials & Methods Results & Discussion Conclusions

Central populationfrom samemountain range

Marginal population

Marginal populationfrom samemountain range

X 6 marginal populations

F1F2

F3

Experimental design:

• Seeds obtained in common garden conditions fromartificial crossings simulating different types of geneflow

Experimental design:

• Ex situ sowing experimentat optimum conditions in growth chamber and greenhouse environment(mother plant x type of cross x block x pop. = 8640 seeds).

• In situ sowing experimentat the locations of the 6 marginal populations(mother plant x type of cross x block x pop. = 24000 seeds)

Introduction Aims Materials & Methods Results & Discussion Conclusions

Introduction Aims Materials & Methods Results & Discussion Conclusions

Ex situ germinationexperiment

F1<F2, F3

F1=F2, F3

Germination = geneflowi + populationj + (geneflow x population)ij + motherplantk(j)

Introduction Aims Materials & Methods Results & Discussion Conclusions

Ex situ germination experiment

RUI AGI CAM SES NAJMOR

F1<F2,F3F1<F2,F3 F1=F2,F3 F1=F2,F3F1=F2,F3

Inbreeding depression No inbreeding depression

F1<F2,F3

Inbreeding depression

F1F2

F3

GuadarramaGredosBéjar

Introduction Aims Materials & Methods Results & Discussion Conclusions

In situ germinationexperiment

F1<F3 F1>F2

F1=F2,F3 F1<F2

Germination = geneflowi + populationj + (geneflow x population)ij + motherplantk(j)

Introduction Aims Materials & Methods Results & Discussion Conclusions

In situ germination experiment

RUI AGI CAM SES NAJMOR

F1>F2F1<F3 F1=F2,F3 F1=F2,F3F1=F2,F3

Inbreeding depression

No inbreeding depression

F1<F2

Adaptation from MOR

F1F2

F3

Maladaptation from RUI

GuadarramaGredosBéjar

Introduction Aims Materials & Methods Results & Discussion Conclusions

In situ germination experiment

RUI AGI CAM SES NAJMOR

Local adaptation (Giménez-Benavides et al., 2007)Inbreeding depression (García-Fernández et al., 2012)

GuadarramaGredosBéjar

Giménez-Benavides L, Escudero A, Iriondo JM. 2007. Ann Bot 99:723-734.García-Fernández A, Iriondo JM, Escudero A.2012. Oikos 121: 1435-1445.

Introduction Aims Materials & Methods Results & Discussion Conclusions

RUI AGI CAM SES NAJMOR

F1F2

F3

F1>F2F1<F3 F1=F2,F3 F1=F2,F3F1=F2,F3

Inbreeding depression

No inbreeding depression

F1<F2

Adaptation from MOR

Maladaptation from RUI

In situ

F1<F2,F3F1<F2,F3 F1=F2,F3 F1=F2,F3

Inbreeding depression No inbreeding depression

F1<F2,F3

Inbreeding depression

Ex situ F1=F2,F3

Introduction Aims Materials & Methods Results & Discussion Conclusions

RUI AGI CAM SES NAJMOR

F1F2

F3

F1>F2F1<F3 F1=F2,F3 F1=F2,F3F1=F2,F3

Inbreeding depression

No inbreeding depression

F1<F2

Adaptation from MOR

Maladaptation from RUI

In situ

F1<F2,F3F1<F2,F3 F1=F2,F3 F1=F2,F3

Inbreeding depression No inbreeding depression

F1<F2,F3

Inbreeding depression

Ex situ F1=F2,F3

He= 0.63FIS= 0.33Ne= 10

He= 0.75FIS= 0.32Ne= 25

He= 0.66FIS= 0.19Ne= 12

He= 0.70FIS= -0.12Ne= inf

He= 0.70FIS= 0.39Ne= 66

He= 0.51FIS= 0.31Ne= 131

Introduction Aims Materials & Methods Results & Discussion Conclusions

RUI AGI CAM SES NAJMOR

F1F2

F3

F1>F2F1<F3 F1=F2,F3 F1=F2,F3F1=F2,F3

Inbreeding depression

No inbreeding depression

F1<F2

Adaptation from MOR

Maladaptation from RUI

In situ

F1<F2,F3F1<F2,F3 F1=F2,F3 F1=F2,F3

Inbreeding depression No inbreeding depression

F1<F2,F3

Inbreeding depression

Ex situ F1=F2,F3

He= 0.63FIS= 0.33Ne= 10

He= 0.75FIS= 0.32Ne= 25

He= 0.66FIS= 0.19Ne= 12

He= 0.70FIS= -0.12Ne= inf

He= 0.70FIS= 0.39Ne= 66

He= 0.51FIS= 0.31Ne= 131

Introduction Aims Materials & Methods Results & Discussion Conclusions

RUI AGI CAM SES NAJMOR

F1F2

F3

F1>F2F1<F3 F1=F2,F3 F1=F2,F3F1=F2,F3

Inbreeding depression

No inbreeding depression

F1<F2

Adaptation from MOR

Maladaptation from RUI

In situ

F1<F2,F3F1<F2,F3 F1=F2,F3 F1=F2,F3

Inbreeding depression No inbreeding depression

F1<F2,F3

Inbreeding depression

Ex situ F1=F2,F3

He= 0.63FIS= 0.33Ne= 10

He= 0.75FIS= 0.32Ne= 25

He= 0.66FIS= 0.19Ne= 12

He= 0.70FIS= -0.12Ne= inf

He= 0.70FIS= 0.39Ne= 66

He= 0.51FIS= 0.31Ne= 131

Leimu R , Fischer M. 2008. PLoS ONE 3: e4010

Introduction Aims Materials & Methods Results & Discussion Conclusions

RUI AGI CAM SES NAJMOR

F1F2

F3

• Seedling survival and size (up to July): No differences between geneflowtreatments

• On-going experiment

In situ

Introduction Aims Materials & Methods Results & Discussion Conclusions

Marginal populations

Central populations

F1F2

F3

Little evidence of adaptive geneflow between marginal populations: • Mimulus laciniatus (Sexton et al., 2011)

Sexton JP, Strauss SY, Rice KJ. 2011. PNAS 108:11704-11709

Introduction Aims Materials & Methods Results & Discussion Conclusions

• Some evidence of central populations providing genetic diversity that reduces inbreeding depression (Holt & Gomulkiewicz, 1997)

• No evidence of maladaptive alleles or gene combinations from central populations(Kirkpatrick & Barton, 1997)

Marginal populations

Central populations

F1F2

F3

Holt RD, Gomulkiewicz R. 1997. Am Nat 149:563-572Kirkpatrick M, Barton NH. 1997. Am Nat 150:1-23

Introduction Aims Materials & Methods Results & Discussion Conclusions

Marginal populations

Central populations

F1F2

F3

Genetic differentiation in functional traits between central and marginal populations:• Tolerance to water stress (García-Fernández et al. 2013).• Flowering phenology: S. ciliata (unpublished results), Armeria caespitosa (Lara-

Romero et al., 2014)

García-Fernandez A, Iriondo JM, Bartels D, Escudero A.2013 Plant Biol 15:93-100.Lara-Romero C, García-Camacho R, Escudero A, Iriondo JM. 2014. Bot J Linn Soc 176:384-395.

Introduction Aims Materials & Methods Results & Discussion Conclusions

Conclusions

1. High incidence of inbreeding depression in marginal populations.

2. Both adaptive/maladaptive geneflow between marginal populations at the germination stage.

3. No maladaptive geneflow between central and marginal populations at the germination stage.

4. Variation of responses to geneflow depending on themarginal population are probably associated to differencesin effective population size, genetic diversity and populationinbreeding.

5. Response to geneflow in a given marginal population is alsodependent on temporal variation of environmentalconditions

Local adaptation versus inbreeding depression in marginal populations of a Mediterranean alpine plant: are they

worthy of conservation in a context of climate change?

Acknowledgements:

• C. Diaz, G. Escribano, S. Prieto, P. Tabares, S. Eleazar, L. Cano & L. Martinez • Parque Nacional de la Sierra de Guadarrama• Parque Regional de la Sierra de Gredos• Reserva de la Biosfera de la Sierras de Béjar y Francia• AdAptA Project CGL2012-33528, Spanish National R&D&I Plan