The Mendelian inheritance of gynomonoecy: insights from Anacyclus hybridizing species

Abstract

Citation: Álvarez, I., A. B. Agudo, A. Herrero, and R. Torices. 2020. The Mendelian inheritance of gynomonoecy: insights from Anacyclus hybridizing species. PREMISE:Gynomonoecy is an infrequent sexual system in angiosperms, although widely represented within the Asteraceae family. Currently, the hypothesis of two nuclear loci controling gynomonoecy is the most accepted. However, the genic interactions are still uncertain. Anacyclus clavatus, A. homogamos, and A. valentinus differ in their sexual system and floral traits. Here, we investigate the inheritance of gynomonoecy in this model system to understand its prevalence in the family. METHODS:We selected six natural populations (two per species) for intra-and interspecific experimental crosses, and generated a total of 1123 individuals from the F 1 generation, F 2 , and backcrosses for sexual system characterization. The frequency of gynomonoecy observed for each cross was tested to fit different possible hypotheses of genic interaction. Additionally, the breeding system and the degree of reproductive isolation between these species were assessed. RESULTS: Complementary epistasis, in which two dominant alleles are required for trait expression, explained the frequencies of gynomonoecy observed across all generations. The heterozygosity inferred in Anacyclus valentinus, as well as its lower and variable seed set, is congruent with its hybrid origin.CONCLUSIONS: In our model system gynomonoecy is controlled by complementary epistasis of two genes. A common origin of this sexual system in Asteraceae, in which genic duplications, mutations, and hybridization between lineages played a key role, is hypothesized whereas independent evolutionary pathways and possibly diverse underlying genetic factors are suggested for gynomonoecy expression in other angiosperm families.

Unravelling plant diversification: Intraspecific genetic differentiation in hybridizingAnacyclusspecies in the western Mediterranean Basin

“…In previous phylogenetic analyses of the genus Anacyclus based on nrDNA and cpDNA sequences (Oberprieler, 2004; Vitales et al, 2018), none of the three study Anayclus species were sisters, although in both cases, A. clavatus and A. valentinus were more closely related to each other than to A. homogamos . Recent evidence also supported the divergence between these three species, such as the significant differences in their genome sizes (Agudo et al, 2019) and the partial post‐zygotic reproductive barriers between them (Álvarez et al, 2020). This study provided additional support to the recognition of these three Anacyclus species, but also brought to light the complexity posed by gene flow among them and the necessity of a thorough review of their diagnostic characters.…”

“…For example, A. valentinus had the lowest genetic diversity among all studied species, despite occurring across a large area along the Iberian and North African Mediterranean coast. In A. valentinus , inbreeding and isolation seem unlikely because it is self‐incompatible (Álvarez et al, 2020) and mostly occurs along roadsides. Moreover, the inbreeding coefficient ( F IS ) for A. valentinus did not indicate an excess of homozygosis, and the AMOVA showed a structure congruent with connected populations.…”

“…For example, Anacyclus clavatus occurs in both coastal and inland areas across the region, indicating that the species can cope with a gradient of Mediterranean subclimates mainly characterized by the severity of winter conditions from mild coastal areas to cold inland areas. In contrast, A. valentinus and A. homogamos are distributed in areas with particular environmental conditions: A. valentinus mainly occupies areas along the coast or with a strong coastal influence, whereas A. homogamos is mostly restricted to the Atlas region in Morocco (Álvarez et al, 2020).…”

“…Although the existence of current gene flow between these species has never been addressed, interspecific hybridization, which would be mediated by the active pollinator community visiting Anacyclus populations (Cerca et al, 2019) was supported by analyses on genome size (Agudo et al, 2019) and ribosomal sites variation (Rosato et al, 2017) of A. clavatus and A. valentinus populations. In our recent investigations including intra‐ and interspecific experimental crosses between A. clavatus , A. homogamos , and A. valentinus , Álvarez et al (2020) found that parents, second‐generation (F 2 ) hybrids, and backcrosses may show similar phenotypes. This highlights the relevance that interspecific hybridization may have on the phenotypic variation in this species complex.…”

“…The genus Anacyclus (Anthemideae, Asteraceae) encompasses eight species of herbs, mostly growing in open anthropic environments, with their center of diversification in western Mediterranean Basin (Humphries, 1979;Vitales et al, 2018). From an evolutionary viewpoint, Anacyclus has been an object of study due to its diversity of floral phenotypes at the species (Humphries, 1981;Bello et al, 2013Bello et al, , 2017Álvarez et al, 2020) and population levels (Agudo et al, 2019;Cerca et al, 2019), including various sexual systems and female flower shapes, colors, and sizes. Interspecific hybridization is likely responsible of such a high diversity of floral phenotypes because most of the Anacyclus species are interfertile (Humphries, 1981;Álvarez et al, 2020) and show some degree of spatial overlap in their distributions.…”