Relatedness-dependent cross-fertility in tropical rainforest trees and the nature of species boundaries (Sri Lanka, Syzygium rubicundum, Shorea cordifolia)

Understanding the spatial scale and genetic basis of interfertility in nature yields insight into the scale and causes of reproductive isolation within species and the nature of species boundaries. For each of two tree species occurring in Sri Lanka's fragmented rainforests [Syzygium rubicundum (Myrtaceae) and Shorea cordifolia (Dipterocarpaceae)], I hand-crossed three maternal trees with five pollen donors ranging from self to donors occurring in separate forests 12 km (S. rubicundum) and 35 kin (Sh. cordifolia) away. Cross-fertility measures included rates of fruit set, seed germination, and survivorship and growth of seedlings over one year. Cross-fertility was optimized between trees occurring within the same forest, but separated by one to several km. The relative reduction in cross-fertility between nearest neighbors was significant for S. rubicundum, but not for Sh. cordifolia. For both species, cross-fertility was significantly reduced where mates occurred in separate forests. Using seven polymorphic microsatellite loci developed for Sh. cordifolia, 190 adults were genotyped from seven populations representing the full geographic range of the species. Mean number of alleles and gene diversity (HE) per locus were 13 and 0.69. Genetic differentiation among populations was low (FST = 0.031), but significant, and did not fit a strict isolation by distance model. Within a population, relatedness of near-neighbor trees was not significant. The relationship between pairwise relatedness and cross-fertility overall fit a quadratic model, however, thus supporting a genetic basis for the reduced cross-fertility observed in both nearest-neighbor and between-forest crosses (i.e., inbreeding and outbreeding depression, respectively). Comparing rates of change over 40 km in cross-fertility and genetic distance at neutral loci revealed that outbreeding depression observed in between-forest crosses is likely enhanced by a selectively heterogeneous environment. For Sh. cordifolia, cross-fertility with a close relative, Sh. megistophylla, exceeded that within species. Cross-fertility between Sh. cordifolia and naturally occurring Sh. cordifolia x Sh. megistophylla hybrids, however, was low. Paternity analysis revealed that hybrids backcross naturally with both parental species. The homogenizing effects of introgressive hybridization in this group, if it occurs, may be countered by selection against intermediate morphotypes. The relationship between genetic similarity and cross-fertility appears to be under different influences at the infra- and supraspecific levels.