Phylogenomic analysis reveals multiple evolutionary origins of selfing from outcrossing in a lineage of heterostylous plants

Abstract

Evolutionary transitions from outcrossing to selfing often occur in heterostylous plants. Selfing homostyles originate within distylous populations and frequently evolve to become reproductively isolated species. We investigated this process in 10 species of Primula section Obconicolisteri using phylogenomic approaches and inferred how often homostyly originated from distyly and its consequences for population genetic diversity and floral trait evolution.We estimated phylogenetic relationships and reconstructed character evolution using the whole plastome comprised of 76 protein-coding genes. To investigate mating patterns and genetic diversity we screened 15 microsatellite loci in 40 populations. We compared floral traits among distylous and homostylous populations to determine how phenotypically differentiated homostyles were from their distylous ancestors.Section Obconicolisteri was monophyletic and we estimated multiple independent transitions from distyly to homostyly. High selfing rates characterised homostylous populations and this was associated with reduced genetic diversity. Flower size and pollen production were reduced in homostylous populations, but pollen size was significantly larger in some homostyles than in distylous morphs.Repeated transitions to selfing in section Obconicolisteri are likely to have been fostered by the complex montane environments that species occupy. Unsatisfactory pollinator service is likely to have promoted reproductive assurance in homostyles leading to subsequent population divergence through isolation.

Temporal Distinction between Male and Female Floral Organ Development in Nicotiana tabacum cv. Xanthi (Solanaceae)

“…Selfing is commonly found in diverse groups of angiosperms and functions in different forms, including geitonogamy (pollen is transferred to a different flower on the same plant) [12,13], autogamy (pollen is deposited on the stigma of the same flower during floral development), and cleistogamy (obligated self-pollination in closed, bud-like flowers) [3,9]. The evolutionary transition from Plants 2020, 9, 127 2 of 23 outcrossing to selfing has been widely studied in many systems [14]. Although selfing may have an advantage over outcrossing under various environmental and reproductive conditions [15,16], multiple mechanisms have been demonstrated to prevent inbreeding depression caused by selfing [17,18].…”

The ecology, evolution, and genetics of plant reproductive systems

“…Examining the breakdown of distyly within a section of Primula , Zhong et al . (, in this issue pp. 1290–1303) find evidence for multiple independent transitions to homostyly, accompanied by high rates of selfing and reductions in flower size and pollen output, in agreement with the notion of the selfing syndrome.…”

‘A most complex marriage arrangement’: recent advances on heterostyly and unresolved questions

“…Most species are either dimorphic or monomorphic for style condition, limiting efforts to determine the population‐level mechanisms favouring homostyle spread. However, recent investigations (Yuan et al ., , ; Zhou et al ., ; Zhong et al ., ) on subalpine, self‐compatible Primula species from southwest China, in which distylous, homostylous and mixed (distylous and homostylous morphs) populations occur, have provided valuable insights into the breakdown process.…”

“…Second, how do transitions in mating system influence population genetic structure and patterns of genetic diversity? Investigations of the genomic consequences of transitions to selfing via homostyle evolution have only just begun (Arunkumar et al ., ; Zhong et al ., ) and additional work would undoubtedly shed light on how changes in mating system affect genome evolution. Third, why and how do some distylous lineages evolve separate sexes?…”