Intercontinental dispersal and whole‐genome duplication contribute to loss of self‐incompatibility in a polyploid complex

Abstract

When species are subject to population bottlenecks arising through multiple factors, each factor can contribute to self-incompatibility loss. In a widespread polyploid complex, the loss of self-incompatibility can be predicted by the cumulative effects of whole-genome duplication and intercontinental dispersal.

Is selfing a reproductive assurance promoting polyploid establishment? Reduced fitness, leaky self‐incompatibility and lower inbreeding depression in neotetraploids

“…In diploids, the haploid gametophyte expresses a single protein and is arrested if recognized by S‐RNases in the pistil; however, tetraploids will produce a mixture of homoallelic and heteroallelic gametophytes and self‐fertilization will be reduced but not eliminated. This mechanism is consistent with incompatibility breakdown in other Campanulaceae (Sutherland et al., ) and with leaky self‐incompatibility observed in J. maritima neotetraploids.…”

“…Breakdown of gametophytic self‐incompatibility has been described as a direct result of genome duplications (e.g., Solanaceae, Rosaceae and other families; Lewis, ; Pandey et al., ; Entani et al., ; Adachi et al., ; Sutherland et al., ), in which pollen tubes containing two copies of the same pollen S‐allele (homoallelic) are arrested if the cognate S‐RNase is present in the pistil, while pollen grains containing two different pollen S‐alleles (heteroallelic) are compatible and thus are allowed to fertilize (de Nettancourt, ; Entani et al., ; Luu et al., ), although accumulation of non‐functional S haplotypes has also been shown (e.g., sour cherry; Hauck et al., ; Tao and Lezzoni, ). In diploids, the haploid gametophyte expresses a single protein and is arrested if recognized by S‐RNases in the pistil; however, tetraploids will produce a mixture of homoallelic and heteroallelic gametophytes and self‐fertilization will be reduced but not eliminated.…”

“…Continuous self‐reproduction increases the level of homozygosity, exposing deleterious recessive mutations and, consequently, causing reduced fitness on inbred progeny (Charlesworth and Charlesworth, ; Lynch and Walsh, ; Stone, ). In J. maritima , the high proportion of self‐incompatible plants and presence of some partially self‐compatible ones suggest that, while selfing may represent a reproductive assurance being strongly favored in initial generations (e.g., after polyploid formation or long‐distance dispersal; Ozimec and Husband, ; Costa et al., ; Sutherland et al., ), it could be a transient state (Schemske and Lande, ), with outcross being favored in future scenarios in case inbreeding depression levels increase (Ozimec and Husband, ). Thus, an intermediate breakdown of the SI system in some J. maritima individuals may benefit neopolyploid establishment, enabling the formation of some viable offspring, while maintaining the capacity for outcrossing (Lloyd, ).…”

“…Still, the association between self‐compatibility and polyploidy is not always clear and the direct effects of genome duplications in mating systems and their role in neopolyploid establishment are still largely unexplored (Mable, ; Husband et al., ). Self‐compatibility is a labile character that evolved repeatedly, according to the plant context in a given moment (Barret, ; Kalisz et al., ; Sutherland et al., ), and the strength of the self‐incompatibility system was shown to vary within and between populations (e.g., Johnston and Schoen, ; Cook and Soltis, , ; Mable, ; Brennan et al., ; Costa et al., ). Thus, a complete shift to self‐compatibility might not be a necessary condition at initial stages of polyploid emergence; instead, partial self‐compatibility could be enough to reduce the problems of reproductive assurance in newly arisen polyploid individuals (Mable, ; Husband et al., ).…”

Genome Size Variation within Species of Chinese Jujube (Ziziphus jujuba Mill.) and Its Wild Ancestor Sour Jujube (Z. acidojujuba Cheng et Liu)

“…The main path of polyploidization is whole-genome duplication (WGD). With the completion of a large number of plant genome sequencing projects, it has been found that WGD events have occurred in most plant evolutionary processes [21,[47][48][49]. The evolutionary process of polyploidization can be roughly divided into three stages [50].…”