The ecology, evolution, and biogeography of dioecy in the genus Solanum: With paradigms from the strong dioecy in Solanum polygamum, to the unsuspected and cryptic dioecy in Solanum conocarpum

Abstract

Confirmed dioecy in at least 15 solanums is distributed across the genus, with perhaps 6 independent origins, and with crypticity in the form of morphologically hermaphroditic, but functionally unisexual, flowers characterizing all species. Dioecy is not more strongly associated with islands. Inaperturate pollen in pistillate flowers characterizes almost all, but not the two dioecious species studied herein. Dioecy in both species indicates leakiness (rare hermaphroditic flowers on male plants) that helps explain island colonization and radiation. Leakiness allowed confirmation-usually impossible for dioecious species-of self-compatibility for S. polygamum, and thus support for the hypothesis that dioecy evolved to promote outcrossing.

Inferring the genetic basis of sex determination from the genome of a dioecious nightshade

“…Given that sexspecificity of gene expression is expected to accumulate with time since the origin of sexual dimorphism (Ellegren and Parsch 2007), the observation that few genes show sex-biased expression is consistent with a young sex-determination system. This very modest genomic and transcriptomic divergence between the sexes is consistent with the subtle morphological differentiation between male and female flowers, which is among the least pronounced in the dioecious nightshades (Anderson, et al 2015).…”

“…Although the economically important, highly speciose (~2000 species) plant genus Solanum contains fewer than 20 documented dioecious species, dioecy is estimated to have arisen independently at least 4 times (Anderson, et al 2015). Many of these transitions appear to involve common phenotypic features, most notably the development of inaperturate pollen in female individuals and dramatic reduction of the pistil in male flowers (Anderson, et al 2015).…”

“…As such, the resources generated here provide a valuable framework for examining additional transitions to dioecy in the highly speciose genus, including a high-quality assembled genome, transcriptome characterization for annotation and gene expression analyses, and a set of candidate loci for directed exploration in parallel systems. Because most dioecious nightshades have similar sexual traits, including inaperturate pollen in the stamens of female flowers (Anderson, et al 2015), addressing the parallel origins of dioecy in this group can also address whether these transitions have followed convergent paths at genomic, genetic, and developmental levels. In conjunction with the S. appendiculatum genome, sequence data from other dioecious Solanum species can be used to dissect these parallel origins of sex determination in Solanum, including whether these exhibit similar genomic features (in terms of the number, size, and distribution of emerging sexdetermination regions), draw on the same kinds of genomic/genetic changes (i.e.…”

“…While most of the nearly 2000 species in the genus are hermaphroditic, there are a number of cases of dioecy, andromonoecy (in which male and hermaphrodite flowers occur separately on the same plant), and even sexually fluid species (Anderson 1979;Symon 1979;Symon 1981;Anderson and Levine 1982;Levine and Anderson 1986;Whalen and Costich 1986;Anderson and Symon 1989;Anderson, et al 2015;McDonnell, et al 2019). Of these, there are 15-20 clearly dioecious Solanum species (Anderson, et al 2015), and their distribution across the phylogeny of the genus suggests that dioecy has independently evolved at least four times (that is, dioecious species appear in four different sections: one in the potato group, one in Dulcamaroid, two in Geminata, and 14 in Leptostemonum (Knapp, et al 2004;Anderson, et al 2015)). Interestingly, in all the dioecious species, female flowers still produce anthers, and the majority of the anthers on the female flowers also include pollen (Anderson, et al 2015).…”

“…Of these, there are 15-20 clearly dioecious Solanum species (Anderson, et al 2015), and their distribution across the phylogeny of the genus suggests that dioecy has independently evolved at least four times (that is, dioecious species appear in four different sections: one in the potato group, one in Dulcamaroid, two in Geminata, and 14 in Leptostemonum (Knapp, et al 2004;Anderson, et al 2015)). Interestingly, in all the dioecious species, female flowers still produce anthers, and the majority of the anthers on the female flowers also include pollen (Anderson, et al 2015). In spite of high viability (stainability) of that pollen, and the presence of many of the same internal constituents as the pollen from male flowers, the pollen grains do not function in the usual way.…”