Introduction
Understanding the factors that drive patterns of genetic variation among
plant populations is central in biology because genetic diversity is the
raw material on which evolution acts. Quantifying population
differentiation, which is most frequently done using the fixation index
FST (Wright,1951; see Holsinger & Weir, 2009; Meirmans
& Hedrick, 2011 for a review of FST and related
metrics), is important for understanding the first stages of allopatric
speciation (Harvey, Singhal, & Rabosky, 2019; Templeton, 1981), as well
as the basis of local adaptation (Leimu & Fischer, 2008; Linhart &
Grant, 1996), and provides critical information for conservation
genetics (Ellstrand, 1992; Ellstrand & Elam, 1993; Kramer & Havens,
2009). Life history traits are expected to influence population genetic
structure in seed plants (Duminil et al., 2007; Hamrick & Godt, 1996;
Loveless & Hamrick, 1984). However, previous studies have given
conflicting results as to the importance of specific traits, such as
pollination mode, seed dispersal mode, mating system, and growth form
(e.g., Duminil et al., 2007; Hamrick & Godt, 1996), and only one study
has compared patterns of FST variation between
latitudinal regions (Dick, Hardy, Jones, & Petit, 2008). Furthermore,
little is known about the relative importance of these factors. Below,
we discuss prior evidence for each of these factors in turn, and then
detail our approach to test them all together in a single analysis that
also accounts for phylogenetic relatedness.
Pollination mode is predicted to affect population genetic structure,
because pollen dispersal is critical to moving alleles between plant
populations. Previous reviews have lumped different pollination
mutualists together as animal pollination and compared them to wind
pollination (Hamrick, Godt, & Sherman-Broyles, 1992; Loveless &
Hamrick, 1984), revealing that wind tends to reduce genetic structure.
Although the idea has not been tested on a broad scale, it has long been
thought that different types of animal pollinators should also lead to
differences in population genetic structure due to differences in their
movement patterns and pollen carry-over capacity (Castellanos, Wilson,
& Thomson, 2003). In fact, direct measures of pollen dispersal reveal
that volant vertebrates and large bees transport larger proportions of
pollen from individual trees to longer geographic distances than small
insects (Dick et al. , 2008). Given these results, we predict that
small insects restrict gene flow among plant populations and increase
FST, compared to large insects, vertebrates, or wind.
Seed dispersal mode is also expected to influence plant population
genetic structure because, like pollination mode, it directly affects
the movement of alleles and thus gene flow among populations. Strong
evidence suggests that limited dispersal increases fine-scale spatial
genetic structure in plants (Gelmi‐Candusso, Heymann, & Heer, 2017) and
in other organisms (Aguillon et al., 2017), which in consequence might
scale up and lead to greater population genetic structure (Hamrick &
Trapnell, 2011). In fact, reviews of the allozyme literature suggest
that seed dispersal by wind and ectozoochory results in lower
FST than dispersal by gravity and endozoochory due to
greater gene flow among populations from long distance dispersal events
(Hamrick & Godt, 1996; Hamrick, Murawski, & Nason, 1993). However,
Duminil et al. (2007) found that dispersal mode was not a significant
predictor of FST. The lack of consistency among studies
encourages further work with larger sample sizes to fully understand the
role of seed dispersal mechanisms on population genetic structure.
Unlike pollination and seed dispersal modes, the effect of mating system
on plant population genetic structure has been well-established in
previous broad-scale studies (Duminil et al., 2007; Loveless & Hamrick,
1984), which suggest that it is the most important predictor of
FST variation. Mating system affects inbreeding, which
lowers within-population variation, inflating between-population
FST values (Charlesworth, 2003). Duminil, Hardy, and
Petit (2009) found that the outcrossing rate and the inbreeding
coefficient, which measures biparental inbreeding and selfing, are both
significant predictors of FST in seed plants. Both
selfing and inbreeding increase inbreeding depression and induce purging
of deleterious alleles, reducing effective population size and
increasing genetic drift, which can ultimately lead to fixation of
different alleles in different populations (Angeloni, Ouborg, & Leimu,
2011; Wright, Ness, Foxe, & Barrett, 2008). In contrast, outcrossing
increases gene flow within populations, potentially intensifying
pollen-mediated gene flow among populations, which counteracts genetic
drift and thus decreases population genetic structure (Duminil et al.,
2009; Ellstrand, 2014).
Growth form is also an important predictor of population genetic
structure. Broad-scale analyses (Duminil et al., 2009; Hamrick et al.,
1992) have found strong associations between growth form and
FST, with woody plants tending to have lower
FST than herbaceous plants. The mechanism that causes
this association is unclear, however, and may actually be driven by
correlations between growth form and other factors. For example, Duminil
et al. (2009) found that growth form only affects FSTindirectly, through its influence on outcrossing rate
(tm) and inbreeding coefficient (FIS);
woody growth form is associated with greater tm and
lower FIS. However, Hamrick and Godt (1996) reviewed the
allozyme literature for over 300 species and found that when considering
outcrossing plants, woody plants show lower levels of
FST than herbs, which suggests that growth form directly
affects gene flow among populations, decreasing population genetic
structure. This could be because in trees greater geographic distance is
presumably required for genetic differences to be detected among
populations than in herbs, given that trees are larger than herbs. Thus,
when considered at similar geographic scales, we predict that herbs have
populations with greater genetic differentiation than trees.
Finally, the latitudinal region in which a plant occurs could also
affect its population genetic structure due to differences among regions
in spatial and climatic landscapes. In general, geographic heterogeneity
and seasonal asynchrony over short distances are considerably higher in
the tropics than in the temperate zones (Esquerré, Brennan, Catullo,
Torres‐Pérez, & Keogh, 2019; Ricklefs, 1977; Stein, Gerstner, & Kreft,
2014), which may act to disrupt mating among conspecific subpopulations,
and thus limit gene flow (Martin, Bonier, Moore, & Tewksbury, 2009;
Quintero, González-Caro, Zalamea, & Cadena, 2014). Additionally,
genetic drift could have a more prominent role in the tropics than in
the temperate zones, due to the fact that most species in the tropics
occur at low population densities and thus should have lower effective
population sizes than in temperate zones (Dick et al., 2008; ter Steege
et al., 2013). In fact, although their sample size was limited and
phylogenetic autocorrelation was not accounted for, Dick et al. (2008)
found that tropical trees have on average higher FSTvalues than temperate trees. Given all of the above effects, we predict
that FST is higher in the tropics than in the temperate
zones.
Previous studies have not included all of the aforementioned factors
together when modeling patterns of population genetic structure in seed
plants (Duminil et al., 2007; Hamrick et al., 1992; Hamrick & Godt,
1996; Loveless & Hamrick, 1984; Nybom & Bartish, 2000). Furthermore,
the most thorough study of FST in seed plants was over a
decade ago (Duminil et al., 2007) and thus could not take advantage of
the wealth of population genetic studies published since then. Here we
reviewed publications to assemble a 337-species database of seed plants
with the goal of evaluating the factors predicted to best explain
variation in plant population genetic structure. We
focused on studies that used nuclear markers because their genetic
structure should reflect both pollen and seed movement (due to
biparental inheritance), unlike chloroplast markers, which only reflect
seed movement (due to maternal inheritance) (McCauley, 1994). We
examined five ecological factors, including pollination mode, seed
dispersal mode, mating system, growth form, and latitudinal region,
while controlling for phylogenetic autocorrelation. We also accounted
for variables pertaining to the sampling scheme that have been shown to
affect FST values for plants (Nybom & Bartish, 2000)
and other systems (Blasco-Costa & Poulin, 2013; Pascual, Rives,
Schunter, & Macpherson, 2017; Riginos, Douglas, Jin, Shanahan, &
Treml, 2011); namely, genotyping technique, distance between
populations, and sample size. Using multiple regressions, we asked: (Q1)
What set of life history traits promote population divergence in seed
plants? (Q2) Do patterns of variation in FST differ
between latitudinal regions? (Q3) What are the relative importance of
these factors in explaining variation in FST?