Breeding systems, hybridization and continuing evolution in Avon Gorge Sorbus

Abstract

Background and aims: Interspecific hybridization and polyploidy are key processes in plant evolution and are responsible for ongoing genetic diversification in the genus Sorbus (Rosaceae). The Avon Gorge, Bristol, UK, is a world 'hotspot' for Sorbus diversity and home to diploid sexual species and polyploid apomictic species. This research investigated how mating system variation, hybridization and polyploidy interact to generate this biological diversity.

Methods: Mating systems of diploid, triploid and tetraploid Sorbus taxa were analysed using pollen tube growth and seed set assays from controlled pollinations, and parent-offspring genotyping of progeny from open and manual pollinations.

Key results: Diploid Sorbus are outcrossing and self-incompatible (SI). Triploid taxa are pseudogamous apomicts and genetically invariable, but because they also display self-incompatibility, apomictic seed set requires pollen from other Sorbus taxa - a phenomenon which offers direct opportunities for hybridization. In contrast tetraploid taxa are pseudogamous but self-compatible, so do not have the same obligate requirement for intertaxon pollination.

Conclusions: The mating inter-relationships among Avon Gorge Sorbus taxa are complex and are the driving force for hybridization and ongoing genetic diversification. In particular, the presence of self-incompatibility in triploid pseudogamous apomicts imposes a requirement for interspecific cross-pollination, thereby facilitating continuing diversification and evolution through rare sexual hybridization events. This is the first report of naturally occurring pseudogamous apomictic SI plant populations, and we suggest that interspecific pollination, in combination with a relaxed endosperm balance requirement, is the most likely route to the persistence of these populations. We propose that Avon Gorge Sorbus represents a model system for studying the establishment and persistence of SI apomicts in natural populations.

Fig. 1.

Flowers of S. aria at various stages of opening; flowers at the ‘balloon’ stage (indicated by white arrows) are still in bud, but they are larger and whiter in colour than flowers at ‘bud stage’ because they are nearer to opening (scale bar = 5 mm).

Fig. 2.

Example images from pollen tube analysis (si, stigma; st, style; h, hairs; o, ovule). (A) Incompatible combination from self-pollination of S. whiteana; arrows indicate that growth of pollen tubes has terminated in the upper parts of the styles (ovules have been removed from the styles). (B) Compatible combination from S. aria pollination of S. whiteana; arrows indicate pollen tube growth continues into the base of the styles. (C) Typically swollen tips of pollen tubes (arrows) that have ended incompatibly in the style of a self-pollinated S. whiteana. (D) Compatible pollen tubes (arrows) in the base of the style from S. leighensis pollinated by S. porrigentiformis. (E, F) Pollen tubes (arrows) that have penetrated ovules of S. whiteana pollinated by S. aria. Scale bars: (A, B, E, F) = 1 mm; (C, D) = 0·2 mm.

Fig. 3.

Proportion of compatible pollinations based on pollen tube growth (A) and seed set (B). The horizontal axis gives the type of pollination combination carried out. Combinations resulting in the production of no compatible pollen tubes or seeds are indicated by 0 to distinguish them from mating combinations that were not tested (indicated by n/t). For each pollination category, taxa occur in the same order across the chart, as shown in the chart legend (left to right). Numbers below bars indicate the total number of crosses carried out for a particular mating combination.