Oecologia (1998) 117:342±352 Ó Springer-Verlag 1998 Luc Gigord á Claire Lavigne á Jacqui A. Shyko Partial self-incompatibility and inbreeding depression in a native tree species of La ReÂunion (Indian Ocean) Received: 2 March 1998 / Accepted: 3 August 1998 Abstract We investigated the reproductive system of that D. acutangula possesses an incompatibility system the threatened taxon Dombeya acutangula ssp. acu- similar to that found in other Sterculiaceae species such tangula Cav. (Sterculiaceae), an endemic tree of the as Theobroma cacao L. Such an incompatibility system Mascarene archipelago (Indian Ocean). A controlled allows a certain amount of sel®ng, and dierent indi- crossing experiment was performed in two natural viduals vary in their degree of self-incompatibility. The populations located in the remnants of the low-eleva- low success of crosses among close neighbours in one tion dry forest on the island of La Re union. Active population suggests that there was spatial structure for pollination, probably mainly by insects, was necessary incompatibility alleles in that population. This could for reproduction in this species. Individuals varied in partly explain the decline of the species in fragmented their degree of self-sterility from 0 to 100%. Out- and disturbed habitats, since relatedness at incompati- crossing between nearby individuals produced lower bility loci may increase in small or isolated population seed set than did crosses between more distant indi- and thus reduce mate availability. viduals within one of the two tested populations. The variation in reproductive success on sel®ng and in the Key words Dombeya acutangula ssp. acutangula á dierent types of crosses could result from inbreeding Island á Habitat fragmentation á Conservation á depression causing embryo death, and we provide evi- Crossing experiment dence that progenies from sel®ng have lower seed size and quality. However, for inbreeding depression to account for the dramatic variation in seed set found in Introduction our crossing experiment, the distribution of genetic load and number of lethal factors required appear A major source of environmental change and distur- unrealistic. We favour an alternative interpretation, bance involves habitat fragmentation, which disrupts normal biological and physical ecosystem processes (Saunders et al. 1991; Noss and Csuti 1994), and often L. Gigord leads to a decrease in population size thereby increasing Laboratoire de Biologie et Physiologie Ve ge tales, random genetic drift and inbreeding depression, de- Faculte des Sciences, Universite de La Re union, creasing interpopulation gene ¯ow and increasing the 15 Avenue Rene Cassin, F-97715 Sainte-Clotilde Cedex 09, Ile de La Re union, France probability of local extinction of populations within a metapopulation (Gilpin 1991; Young et al. 1996). In- J.A. Shyko Laboratoire d'Evolution et Syste matique, trinsic population processes in small populations may Universite Paris-Sud [CNRS (URA 2154)], BaÃtiment 362, result in decreasing population viability (for an overview F-91405 Orsay Cedex, France see Soule 1987). While some characteristics may pre- C. Lavigne dispose particular species to persist or even spread under Institut de Biotechnologie des Plantes, changing environmental conditions, others expose some Laboratoire de Phytopathologie Mole culaire, Universite Paris-Sud, species to diculties (Schonewald-Cox 1985); in partic- BaÃtiment 630, F-91405 Orsay Cedex, France ular, in ¯owering plants, the reproductive and pollina- Present address: tion system may in¯uence the viability of small L. Gigord (&) populations, but these eects have not received sucient Laboratoire d'Evolution et Syste matique, Universite Paris XI, BaÃtiment 362, F-91405 Orsay Cedex, France, attention to date (Menges 1991). e-mail: [email protected], The rate of outcrossing versus self-pollination may Tel.: +33-1-69156115, Fax: +33-1-691 57353 be an important factor for population viability (Barrett 343 and Kohn 1991). Plants possess many dierent mech- become extinct and currently approximately 50 are anisms that promote outbreeding, including genetic considered threatened (Bosser et al. 1976; Dupont et al. self-incompatibility systems that preclude the produc- 1989). tion of inbred zygotes after self-pollination and crosses Dombeya acutangula (sensu lato) is a widely distrib- among some related individuals. Self-incompatible uted tree in Africa (Seyani 1991), Madagascar (Are neÁ s species are expected to harbour higher genetic load 1959) and islands of the Indian Ocean (Friedmann 1987). than species that habitually inbreed (Barrett and On La Re union, it is only represented by the endemic Charlesworth 1991) and should suer more from in- subspecies D. acutangula ssp. acutangula (Sterculiaceae) breeding depression than would autogamous species which is considered threatened (Dupont et al. 1989). On (Charlesworth et al. 1990). In fact, inbreeding depres- Mauritius and Rodrigues, the species is nearly extinct sion is found in the rare ospring produced by sel®ng (Bosser et al. 1976). On La Re union, the species can be in largely self-incompatible species (Manasse and found throughout the low-elevation areas of human Pinney 1991; Ramsey and Vaughton 1996). In small habitation and only isolated fragments of natural pop- populations resulting from habitat fragmentation this ulations remain. A previous study (Gigord et al., in press) eect should be particularly problematic because small has shown that the reproductive output of the species is populations are more prone to the accumulations of signi®cantly aected by habitat fragmentation. Further- deleterious alleles than are large populations (Hauser more, anecdotal reports of isolated individuals of D. et al. 1994; Lynch et al. 1995). acutangula ssp. acutangula that produced no seeds de- There are two typical self-incompatibility systems: spite active pollinator visitation suggested that this spe- sporophytic systems, where matings between parent cies might exhibit a self-incompatibility system that could plants that share any alleles at the self-incompatibility contribute to its decline in natural habitats in locus are prevented, and gametophytic systems, where La Re union. We therefore investigated the reproductive pollen growth fails if it shares an allele with the re- system of this species using a series of controlled crosses. cipient plant (de Nettancourt 1977). Other incomplete The goal of this study was to determine whether this self-incompatibility systems, however, exist. These may species is self-compatible and whether it requires pollen be leaky, such that sel®ng or crosses between indi- vectors for fertilisation. We further tested if distances viduals bearing the same incompatibility alleles result between pollen donors and recipient plants in¯uenced in seed (Reinartz and Les 1994). Incomplete incom- seed production and components of progeny ®tness. patibility will therefore expose deleterious recessive This was done to investigate the potential relatedness alleles to selection more often than complete incom- among more or less geographically distant individuals, patibility systems, so the genetic load should be and to determine whether low mate availability and/or reduced by selection. Incompatibility systems aect inbreeding depression may indeed be contributing to the the availability of possible mates. Clearly rare incom- decline of this threatened species. patibility alleles should spread, and high allelic diver- sity occurs for loci governing self-incompatibility (see Richman and Kohn 1996). In small populations, Study species however, even selected alleles can be lost by drift (Kimura 1983), so genetic variability at the incompati- D. acutangula ssp. acutangula Cav. (Sterculiaceae) is a bility locus may decline, thus reducing mate availabi- small tree up to 8 m tall, sometimes ¯owering as a shrub lity. When sel®ng or pollinations between certain as young as 3 years old. Flowering lasts for 2±7 weeks individuals fail to produce seed, either inbreeding between March and May in La Re union. Mature adult depression leading to zygote death or incompatibility plants produce hundreds of large white ¯owers (diame- of the mating can be invoked. ter about 20±30 mm) grouped in cincinnate axillary Island plant species might be particularly prone to in¯orescences of approximately 20 ¯owers. Each ¯ower diculties from habitat change induced by human bears one ovary enclosing ten ovules shared among ®ve activity. They are often bad competitors, low dispersers locules. These ¯owers are protandrous with extrorse and obligatory outcrossers (Janzen 1971; Bawa 1982; anthers, and the pistil becomes receptive 1 day after Baker and Cox 1984; Mueller-Dombois and Loope stamen dehiscence. Pollination is not well documented, 1990), and islands are arenas for the evolution of rare but observations of insect visits in the ®eld and the reproductive systems (Baker 1967). The islands of the production of a large quantity of nectar suggest that Mascarene archipelago (Mauritius, La Re union and plants are mainly pollinated by butter¯ies and a large Rodrigues) are particularly interesting for investigating range of insects such as bees, ants, ladybirds, bumble- this problem because they were free from human in¯u- bees or beetles, and also occasionally by a small endemic ence until the middle of the 16th century, unlike the bird (Zosterops borbonicus Bodaert) known to pollinate Hawaiian archipelago that was colonised a few thou-