Evolution of inbreeding depression in species combining self-incompatibility and partial asexual reproduction

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Evolution of inbreeding depression in species combining self-incompatibility and partial asexual reproduction

Miguel Navascués, Solenn Stoeckel, Stéphanie Mariette

To cite this version:

Miguel Navascués, Solenn Stoeckel, Stéphanie Mariette. Evolution of inbreeding depression in species combining self-incompatibility and partial asexual reproduction. 11. Congress of the European Society of Evolutionary Biology (ESEB), Aug 2007, Uppsala, Sweden. 2007. �hal-02755474�

EVOLUTION OF INBREEDING DEPRESSION IN SPECIES COMBINING SELF-INCOMPATIBILITY AND ASEXUAL REPRODUCTION

Miguel Navascués ¹ , Solenn Stoeckel ² , Stéphanie Mariette ³

1

Laboratoire d’Ecologie UMR 7625 CNRS/ENS/UPMC, 75005 Paris, FRANCE

2

Laboratoire Ecologie, Systématique et Evolution UMR 8079, UPS/CNRS/INAPG/ENGREF, 91405 ORSAY, FRANCE

3

INRA, Unité de Recherche sur les Espèces Fruitières, 33883 VILLENAVE D’ORNON, FRANCE [email protected]

The origin and maintaining of self-incompatibility systems in angiosperms are still debated questions. The level of inbreeding depression in species that show a self-incompatibility system is a key parameter for the maintenance of the system. Several studies were developed to predict when the system can breakdown. A decrease of inbreeding depression, but also a reduction in the number of alleles at the self-incompatibility locus and outcross polenn limitation, are generally associated with that breakdown. Two studies (Chen et al., 1997; Vallejo-Marín & O’Brien, 2007) have suggested that clonality could relieve the main selective pressures favouring the breakdown of self-incompatibility. In this study, we developed a model to simulate the evolution of inbreeding depression in a diploid species that reproduce both asexually and sexually with a self- incompatibility system. Our aim was to answer the following question:

Does clonality allow maintaining self-incompatibility in plants?

Gametophytic self- incompatibility

A₁A₃

A₁A₂ A₃A₄

A₁A₂ A₂ A₁

A₁ A₂ A₁

A₂

Asexual reproduction e.g. sprouting

Balloux F, Lehmann L, De Meeûs T. 2003. The population genetics of clonal and partially clonal diploids. Genetics 164: 1635-1644.

Chen L, James SH, Stace HM. 1997. Self-incompatibility, seed abortion and clonality in the breeding systems of several western Australian Drosera species (Droseraceae). Autralian Journal of Botany 45: 191-201.

Glémin S, Bataillon T, Ronfort J, Mignot A, Olivieri I. 2001. Inbreeding depression in small populations of self-incompatible plants. Genetics 159: 1217-1229.

Vallejo-Marín M, O’Brien HE. 2007. Correlated evolution of self-incompatibility and clonal reproduction in Solanum (Solanaceae). New Phytologist 173: 415-421.

INTRODUCTION INTRODUCTION

DESCRIPTION OF THE MODEL DESCRIPTION OF THE MODEL

RESULTS RESULTS

CONCLUSIONS & PERSPECTIVES CONCLUSIONS & PERSPECTIVES

N diploid

hermaphroditic plants Reproduction system

Clonal with probability c Sexual with probability (1- c )

Gametophytic

self-incompatibility controlled by a S locus

Modelled locus

2 neutral loci S locus

Viability locus causing inbreeding depression

Principal monitored variables For each locus

Observed heterozygosity Expected heterozygosity

Allelic richness

Effective number of alleles

Within population fixation index Linkage disequilibrium between

each pair of loci

Viability locus

Inbreeding depression Mutation load

Frequency

of the deleterious allele

Random sample of one individual

Mutation

μ

_S

for the S locus

μ

_N

for the neutral locus μ

₁

if the allele is A

μ

₂

if the allele is a for the viability locus

Asexual reproduction New individual

that undergoes selection Or sexual reproduction

Random sample of a second individual Sample of a pollen grain

Iteration until a compatible cross is found Zygote that undergoes selection

Until N individuals are formed

0 1 2 3 4 5 6 7 8 9

0 0.5 0.8 0.9 0.95 0.99 0.999 1

Clonality rate Effective

number of alleles

1. Effective number of alleles as a function of clonality

The effective number of alleles at neutral loci (µ

_N

=10

^-3

) increases with clonality. Our results show that the effective number of S alleles decreases with mutation rate (µ

_S

=10

^-3

, µ

_S

=10

^-4

, µ

_S

=10

^-5

) at the S locus but also with clonality.

2. Mutation load as a function of population size and clonality

For a fixed clonality rate, the mean mutation load (selection coefficient=0.1 and dominance coefficient=0.2) increases as population size decreases. For a fixed initial population size, it increases as clonality rate increases (except for N =25 for which it slightly decreases between c =0 and c =0.5).

3. Inbreeding depression as a function of population size and clonality

For low clonality rates ( c <0.8), inbreeding depression decreases when population size decreases. For c <0.8, inbreeding depression is higher in small populations than in large ones. Inbreeding depression increases with clonality rate (except for N =25 for which it slightly decreases between c =0 and c =0.5).

0 2 4 6 8 10 12 14

0 0.5 0.8 0.9 0.95 0.99 1 1 Clonality rate

Inbreeding depression

N=25 N=50 N=75 N=100 N=500 N=1000 0.6

0.8 1 1.2 1.4 1.6 1.8

0 0.5 0.8

Clonality rate Inbreeding

depression

N=25 N=50 N=75 N=100 N=500 N=1000

4. Linkage disequilibrium between the S locus and the

viability locus as a function of population size and clonality

Linkage disequilibrium between all pairs of loci increases when clonality increases. The linkage between the S locus and any other locus was higher than the linkage between the other locus (data not shown).

Clonality favours heterozygosity at all loci (Balloux et al. 2003), homozygotes at the viability locus cannot be produced, and thus eliminated. As a result, the frequency of deleterious alleles (data not shown), mutation load and inbreeding depression increase with clonality. This effect is reinforced in small populations. At the same time, our results showed that a strong linkage disequilibrium is created between the S locus and the viability locus while increasing clonality, this can theoretically also reinforces polymorphism at the viability locus (Glémin et al. 2001). Simulations without self- incompatibility are necessary to disentangle the effect of clonality alone and the effect of self-incompatibility on the viability locus.

As a consequence, clonality can theoretically favours maintaining self-incompatibility in populations. However, since our results also showed that the effective number of S alleles decreased with clonality, this may create cases for which self-incompatibility can breakdown.

Population size=100 0

5 10 15 20 25 30

0 0.5 0.8 0.9 0.95 0.99 0.999 1 Clonality rate

Genetic load

N=25 N=50 N=75 N=100 N=500 N=1000

0 0.2 0.4 0.6 0.8 1 1.2

0 0.5

0.8

0.9

0.95 0.99

0.999 1 Clonality rate

LD S

& V locus

N=25 N=50 N=75 N=100 N=500 N=1000