Possible regional differences in pollen and seeds dispersal: effect on Embothrium coccineum gene flow
Our analysis of the genetic differentiation drivers in E. coccineum identified a significant pattern of isolation by distance (IBD). The existence of IBD indicates that gene flow is limited as geographic distance increases (Wright, 1943), however some level of connectivity was observed between nearby populations, mostly in the Center and South. In other plants, as Dactylis glomerata (Sun et al., 2017) and Protea rapens (Prunier et al., 2017), IBD patterns were detected at similar geographic scale, pointing out opportunities for increased allelic exchange between neighboring populations. Moreover, STRUCTURE, PCA and NJ distance tree analyses, and estimation of pairwise-FST values, showed that populations from the North genetic group of E. coccineum are highly structured. We hypothesize that this population structure differences between localities within the North and the Center-South genetic groups could be, in part, linked to the existence of a more restricted gene flow in the northern part of the distribution.
Plant gene flow may occur via pollen and/or seed dispersal and is directly affected by the species reproductive system (Martins, 1987). The Proteaceae family is mostly composed by outcrossing shrubs and/or small trees presenting patchy, naturally fragmented distribution and moderate levels of genetic diversity (Collins and Rebelo 2006, Souto and Premoli, 2007). These features have led Mathiasen et al., (2007) to consider E. coccineum as a species with low sensitivity to the effects of forest fragmentation due to a predominantly outcrossing breeding system, which may favor pollen exchange among nearby fragments (Rovere and Chalcof 2010). Indeed, genetic erosion by drift in forest patches could be counteracted by pollinator’s movements, reducing inbreeding, and allowing the populations to retain sufficient heterozygosity through a continuous influx of alleles from locally distinct gene pools (Mathiasen et al., 2007). Embothrium coccineum , gene flow is highly dependent on pollinating agents (Mathiasen, 2004; Rovere and Chalcof 2010) and his flowers are visited by more than 20 species, including birds of the orders Passeriformes and Apodiformes, and insects of the orders Hymenoptera, Diptera, Lepidoptera and Coleoptera (Chalcoff, 2008).
The composition of the pollinator assemblage affects both, pollen transport and seed production. In regions with low number of E. coccineum pollinators, pollen limitation can be high, leading to low reproductive efficiency (i.e., few fruits produced in relation to the available flowers) (Chalcoff, 2008). This could translate in populations presenting reduced genetic diversity and high genetic structure due to the lack of genetic exchange (Rovere and Chalcof 2010). Pollinating insects, generally characterized by low migration capacities, are distributed throughout the whole E. coccineum distribution range even if they are more abundant and visit the plants more frequently in populations located in drier and sunnier climates (i.e., North) (Rovere and Chalcof, 2010). Contrastingly, birds, as the hummingbirdSephanoides sephaniodes , are very abundant in southern populations located in areas characterized by cool and humid conditions where they act as major pollinators (Chalcoff, 2008). We propose that differences between North and Center-South of E. coccineumpollinators distribution and behavior could be one of the drivers leading to the observed genetic structure, with a lower dispersal capacity in the north leading to a higher level of structure.
However, other differences between regions, as the level of landscape fragmentation, could also generate the pattern observed in our data set and need to be further tested. In Protea rapens , a widespread Proteaceae from the Cape Floristic Region in South Africa, a genetic split between eastern and western population was observed (Prunier et al., 2017). Changes in the timing of rainfall, from a predominantly winter rainfall in the west, to a more evenly distributed rainfall, during the year in the east were reported in the study region (Schultze, 2007). Prunier et al. (2017) proposed that differences in P. rapens flowering time (Heeleman et al., 2008), linked to rainfall patterns, could hinder gene flow between populations, reinforcing the east-west divide. Differences in climatic conditions along the species distribution range also affect E. coccineum flowering period, with a flowering period beginning later (i.e., November – December) in populations located at high latitude and altitude when compared to the rest of the distribution (i.e., September- October) (Hoffmann, 1997; Chalcoff, 2008; Rovere and Chalcof, 2010). Limited gene flow between populations presenting differences in flowering phenology could also lead in part to the observed pattern of divergence between and within genetic groups, by limiting exchange between close by populations located at contrasting altitude.