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.