Genetic diversity and fitness in small populations of partially asexual, self-incompatible plants

Heredity (2010) 104, 482–492 & 2010 Macmillan Publishers Limited All rights reserved 0018-067X/10 $32.00 ORIGINAL ARTICLE www.nature.com/hdy Genetic diversity and fitness in small populations of partially asexual, self-incompatible plants M Navascués1,2, S Stoeckel3 and S Mariette4 Unidad de Genética, Centro de Investigación Forestal, INIA, Carretera de La Coruña km 7.5, Madrid, Spain; 2Équipe Éco-évolution Mathématique, CNRS, UMR 7625 Écologie et Évolution, Université Pierre et Marie Curie & École Normale Supérieure, Paris, France; 3 UMR Biology of Organisms and Populations applied to Plant Protection, INRA Agrocampus Rennes, Le Rheu, France and 4Unité de Recherche sur les Espèces Fruitières, INRA, Domaine de la Grande Ferrade, Villenave d’Ornon, France 1 How self-incompatibility systems are maintained in plant populations is still a debated issue. Theoretical models predict that self-incompatibility systems break down according to the intensity of inbreeding depression and number of S-alleles. Other studies have explored the function of asexual reproduction in the maintenance of self-incompatibility. However, the population genetics of partially asexual, self-incompatible populations are poorly understood and previous studies have failed to consider all possible effects of asexual reproduction or could only speculate on those effects. In this study, we investigated how partial asexuality may affect genetic diversity at the S-locus and fitness in small self-incompatible populations. A genetic model including an S-locus and a viability locus was developed to perform forward simulations of the evolution of populations of various sizes. Drift combined with partial asexuality produced a decrease in the number of alleles at the S-locus. In addition, an excess of heterozygotes was present in the population, causing an increase in mutation load. This heterozygote excess was enhanced by the self-incompatibility system in small populations. In addition, in highly asexual populations, individuals produced asexually had some fitness advantages over individuals produced sexually, because sexual reproduction produces homozygotes of the deleterious allele, contrary to asexual reproduction. Our results suggest that future research on the function of asexuality for the maintenance of self-incompatibility will need to (1) account for whole-genome fitness (mutation load generated by asexuality, self-incompatibility and drift) and (2) acknowledge that the maintenance of self-incompatibility may not be independent of the maintenance of sex itself. Heredity (2010) 104, 482–492; doi:10.1038/hdy.2009.159; published online 18 November 2009 Keywords: self-incompatibility; asexual reproduction; number of S-alleles; linkage disequilibrium; inbreeding depression; mutation load Introduction Hermaphroditic plant species reproduce with variable rates of selfing, ranging from strict selfing to strict outcrossing (Barrett, 2002). Self-incompatibility (SI) is a reproductive system that prevents self-fertilization. In the case of heteromorphic self-incompatibility, distinct morphologies result in distinct compatibility groups, whereas in the case of homomorphic self-incompatibility, compatible individuals cannot be distinguished by their morphology (de Nettancourt, 1977). Most SI systems depend on physiological mechanisms that prevent pollen germination or pollen tube growth. In sporophytic selfincompatibility (SSI) systems, the compatibility of a pollen grain depends on the diploid genotype of the plant that produced it. In gametophytic self-incompatibility (GSI) systems, the compatibility of a pollen grain depends on its haploid genotype. GSI is more widespread than SSI (Glémin et al., 2001). Correspondence: Dr S Mariette, Unité de Recherche sur les Espèces Fruitières, INRA, Domaine de la Grande Ferrade, 71 avenue Edouard Bourlaux, BP 81, Villenave d’Ornon 33883, France. E-mail: Received 29 April 2009; revised 9 October 2009; accepted 20 October 2009; published online 18 November 2009 Fisher (1941) showed that self-fertilization should have a selective advantage because a selfing genotype will transmit more copies of its genome than a non-selfing genotype (this has been termed the automatic advantage of selfing). However, numerous studies have shown that inbred offspring are less fit than outbred offspring. The relative decrease in the mean fitness of selfed versus outcrossed individuals (inbreeding depression) is generally recognized as the only main factor that counterbalances the selective advantage of selfing (Charlesworth and Charlesworth, 1987). Consequently, the level of inbreeding depression in populations should have a determining function in the evolution of SI systems. Inbreeding depression decreases as population size becomes smaller due to reduced polymorphism for selection to act on (Bataillon and Kirkpatrick, 2000). Charlesworth and Charlesworth (1979) showed that the number of S-alleles also is important in maintaining SI, because a low number of alleles will limit the number of compatible crosses in the population. A decrease in population size can also cause a reduction in the number of S-alleles (Brennan et al., 2003), and a self-compatible mutant can be positively selected for (Reinartz and Les, 1994). Thus, small populations may be particularly prone to the breakdown Asexuality and SI in small populations M Navascués et al 483 of SI due to weak inbreeding depression and low numbers of S-alleles. However, small self-incompatible populations may maintain high levels of inbreeding depression due to a sheltered load of deleterious alleles linked to the S-locus (Glémin et al., 2001). The existence of a sheltered load has been shown experimentally in Solanum carolinense by Stone (2004) and Mena-Alı́ et al. (2009). Overall, under a wide range of conditions, SI can evolve to self-compatibility. In effect, the loss of SI systems is very frequent in plant evolution (Igic et al., 2008). However, the reasons for which some species maintain an SI system whereas other species lose it are not completely understood. It has been suggested that asexual reproduction, ‘when an individual produces new individuals that are genetically identical to the ancestor at all loci in the genome, except at those sites that have experienced somatic mutations’ (de Meeûs et al., 2007), has a function in the maintenance or breakdown of SI. Two studies suggest that asexuality could relieve the main selective pressures that favor the breakdown of SI. First, Chen et al. (1997) showed in Australian Droseraceae that all self-incompatible taxa have effective forms of asexual reproduction, whereas the obligatory sexual annual taxon, Drosera glanduligera, is self-compatible. Their interpretation is that selfincompatible forms accumulate recessive lethal polymorphisms, especially in association with biparental inbreeding generated by elevated levels of asexual reproduction. The hypotheti (...truncated)