Diversification of pollination systems as a function of variation
in floral abundance, community context and pollinator assemblage
I then tested if changes in species abundance associated with the
colonization of new communities, as well as inter-community variation in
plant species composition and pollinator assemblage can drive
pollination system diversification in plant clades. Each simulation
consisted of a new colonist successively invading and adapting to 20
different plant communities, representing the diversification of a plant
clade extending its geographical range. Assuming that 1) there is some
degree of variation in the composition of the different communities and
2) the composition of each community is likely to be most similar to the
community nearest to it in space, the attributes of each new colonized
community (abundance of the new colonist, abundance of the other plant
species, or of the different pollinators) were randomly sampled from a
normal distribution characterized by a mean equal to the average value
of the attributes of the last colonized community. Different sets of 100
simulations were run with different degrees of variation of the normal
distribution from a coefficient of variation of 0.01 to 1, with
increments of 0.01 between sets of simulations (the coefficient of
variation corresponds to the standard deviation standardized to
represent a proportion of variation around the average). Distributions
were truncated at minimum values of 2 (assuming that at least two
individuals are necessary for species survival) to avoid sampling
negative values using the ‘rtruncnorm’ function from the R package
‘truncnorm’ (Mersmann et al. 2018). The initial plant-pollinator
networks used for the simulations were generated in the same way as in
the previous simulations.
Three different sets of simulations were performed in which the invaded
communities varied in either 1) the abundance of the new colonist, 2)
the abundance of the existing plant species in the community and 3) the
abundance of the different pollinator species. The subset of pollinators
on which the colonist evolved toward were recorded for each simulation.
Results
The impact of pollinator abundance and pollen removal rate on plant
pollination success increased with floral abundance, while the impact of
pollen carryover and pollinator specialization decreased with floral
abundance (fig. 1A-D). Overall, the quality component of pollination was
more important for pollination success than the quantity component at
low floral abundance, while the quantity component was more important
for pollination success at high abundance (fig. 1E).
For simulated plant communities in which plant species varied in
abundance, the different species exhibited variable degrees of
specialization within the communities (average number of links ±
standard deviation = 2.17± 0.29) (fig. 2A, B). In contrast, in simulated
plant communities where all plant species were of low abundance, most
species specialized on a limited subset of the available pollinators
(average number of links ± standard deviation = 1.58 ± 0.32) (Fig. 2C,
D). In plant communities composed of abundant plant species, most
species generalized on a high proportion of the pollinators available
(average number of links ± standard deviation = 3.41 ± 0.48) (Fig. 2E,
F).
The simulated plant communities in which species varied in abundance
exhibited more variation in degree of specialization among species
relative to the communities with no variation in plant abundance (Fig.
3A). This effect was more pronounced in communities with high average
floral abundance. The communities with variation in abundance shared
fewer pollinators between plant species (Fig. 3B) and produced more
nested (Fig. 3C) and less connected plant-pollinator networks (Fig. 3D).
Incorporating adaptive foraging produced less connected networks while
high flower constancy of the pollinators had the opposite effect
(Appendix S1).
The subset of available pollinators to which a new plant colonist
evolved was a function of its floral abundance. At very low floral
abundance, the colonist specialized on pollinators weakly exploited by
the other plant species, thereby reducing competition via interspecific
pollen transfer (Fig. 4). These less-preferred pollinators were often
relatively rare and had a low carryover capacity, as pollinators with
high abundance and carryover were generally exploited by several plant
species. From very low to relatively low abundance, there was a tendency
for the new colonist to shift toward specialization on a subset of
pollinators with high carryover rather than low competition. This
pattern was less pronounced when all plant species were of low abundance
and all pollinators were therefore weakly exploited (at average flower
abundance of 100, see Appendix S1). In this case, given that competition
was low for all pollinators, high carryover was favored at both very low
and low abundance. From intermediate to high abundance, the new colonist
favoured more abundant pollinators. Generalization increased with
abundance, but only at very high abundance were the majority of the
available pollinators exploited. Pollinator competition (degree of
specialization of the pollinator) and carryover were opposed such that
pollinators with high carryover capacity were exploited by several plant
species, while pollinators with low carryover capacity were less
exploited. This pattern resulted in plants evolving on pollinators with
less competition in average at high plant abundance relative to low
abundance. Indeed, increased generalization at high abundance resulted
in the incorporation of both pollinators with high carryover and low
competition (specialized pollinators) comparatively to only pollinators
with high carryover (and therefore highly exploited pollinators) at low
abundance.
For the simulated plant clades colonizing new communities, diversity in
pollination systems increased with variation in species abundance within
the clade, as well as with variation in plant community composition and
pollinator assemblage (Fig. 5).
Discussion
Many plant lineages and communities are characterized by high floral
diversity (Van der Niet & Johnson 2012). However, the causes of floral
diversification and specialization remain elusive (Kay & Sargent 2009;
Johnson 2010; Van der Niet & Johnson 2012; Armbruster 2017). Here I
propose that a species’ relative abundance in a community determines the
pollination system offering the optimal evolutionary solution (Fig. 1,
4). Given that abundance is evolutionarily and ecologically labile
(Ricklefs 2010; Loza et al. 2017), shifts in abundance associated
with the colonization of new habitats or geographic ranges could promote
floral diversification. This model complements the Grant-Stebbins model
in which flower diversification results from geographical variation in
pollinator assemblages (Grant & Grant 1965; Stebbins 1970). In this
more holistic view, floral diversification is the result of variability
in pollinator assemblages (Fig. 5c), floral abundance (Fig. 5a), and
plant-community composition (Fig. 5b). This perception considerably
relaxes the conditions under which floral diversification occurs and
offers an explanation for the variability in pollinator use and degree
of specialization within and among communities.
Within communities, the presence of interspecific variation in species
abundance increased diversity in degree of generalization and decreased
niche overlap in pollinator use (Fig. 3). Such variability also
contributed to producing more realistic network structures. Indeed,
while networks from communities without variation in abundance were
frequently less nested and more connected then empirical
plant-pollinator networks, communities with variable species abundance
produced networks with nestedness and connectance within the range of
empirical values (Fig. 3, compared to values of nestedness of 0.59 to
0.98 from 25 plant-pollinator networks in Bascompte et al. 2003
and values of connectance of 0.02 to 0.29 from 29 networks in Olesen &
Jordano 2002).
In the simulated plant communities, flower specialization was observed
at low abundance while generalization was favoured at higher abundance
(Fig. 2A, B, Fig. 4), a pattern consistent with the frequently observed
link between abundance and degree of generalization in plant-pollinator
networks (Jordano et al. 2002; Bascompte et al. 2003;
Vázquez & Aizen 2003). While the cause of this pattern is debated
(Dorado et al. 2011; Fort et al. 2016), the model
presented here suggests that the link between abundance and
generalization can originate from a selective advantage of
generalization at high abundance. Furthermore, simulated plant
communities composed of plant species of low abundance resulted in
widespread specialization, while communities of high abundance species
were associated with generalized pollination (Fig. 2). This observation
is consistent with the widespread floral specialization characterizing
highly diverse plant communities composed mostly of rare species, such
as in Mediterranean and tropical climates (Johnson & Steiner 2000;
Vamosi et al. 2006). In such communities, plants should be under
stronger selective pressure for specialization in order to avoid pollen
loss from inefficient carryover and interspecific pollen transfer
(Feinsinger 1983, Johnson and Steiner 2000).
Interestingly, while at moderately low abundance plants specialized on a
subset of pollinators with high carryover capacity, at very low
abundance the species frequently specialized on pollinators of low
abundance and carryover (Fig. 4). Those pollinators were less exploited
by more abundant plant species, which instead evolved pollination by
abundant and efficient carriers of their pollen, offering a
competition-free space for very rare species. This pattern of plant
community assembly can be explained by the increasing probability of
interspecific visits with increasing plant rarity, exacerbating the
importance of interspecific pollen loss at very low abundance. The
propensity for rare plant species to fill up unexploited pollination
niches has the potential to give rise to the evolution of unique
pollination systems, potentially contributing to the impressive
diversity in modes of pollination characterizing tropical and
Mediterranean communities.
The mathematical model and the simulated plant-pollinator networks
demonstrate that, from low to intermediate abundance, plants should
specialize on a subset of pollinators offering the optimal combination
of pollination quantity and quality components (Fig. 1, 4). However, as
plant abundance increases and most pollinators are not sufficiently
abundant to remove the majority of pollen grains, highly generalized
pollination should be favoured. But what happens at the extreme end of
the plant abundance spectrum, when the entire pollinator community
cannot provide enough visits to prevent pollen limitation? In those
conditions, perhaps the best strategy is for plants to relax their
dependence on biotic pollen vectors. While the evolution of wind
pollination from animal pollination has mostly been attributed to
reduced reliability of animal pollinators, most wind-pollinated plants
are characterized by large population size and high density (Culleyet al. 2002; Friedman & Barrett 2009). Indeed, it seems doubtful
that any combination of pollinators could adequately pollinate the
thousands of flowers per square metre characterizing the bloom of
temperate deciduous trees or Poaceae grasslands. Moreover, despite wind
representing a relatively inefficient system of pollen transport, the
high abundance characterizing most wind-pollinated plants reduces the
importance of pollen vector efficiency.
Several theoretical models emphasize the importance of fitness
trade-offs in the evolution of flower specialization (Aigner 2001;
Sargent & Otto 2006; Muchhala 2007). Such trade-offs are expected to
occur when adaptation to a pollinator decreases the effectiveness of
pollination by other pollinators. However, despite having been detected
in some studies, fitness trade-offs in the effective use of different
pollinators are often weak or absent (see Armbruster 2014, 2017). Hence,
it seems unlikely that floral specialization is the sole result of
trade-offs. Here, similar to Muchhala et al. (2010), who investigated
the role of interspecific pollen transfer in flower specialization, I
demonstrate that specialization can evolve without trade-offs. Rather,
specialization should be advantageous when pollinator quantity is less
limiting than pollinator quality.
When present, fitness trade-offs in the effective use of different
pollinators should increase floral specialization. However, the model
presented here is consistent with the perception that floral
specialization might be governed not only by adaptation to increase
pollen removal and deposition by the most effective pollinator, but also
by the exclusion of less efficient ones (Thomson 2003; Castellanoset al. 2004; Muchhala et al. 2010; Armbruster 2017).
Paralleling evolution toward the most effective pollinator, exclusion of
less efficient pollinators through the evolution of pollinator filters
could produce trade-offs if it also excludes efficient but infrequent
pollinators. In other words, pollinator filters might rarely allow
singling out unwanted pollinators. For instance, the evolution of long
nectar spurs prevents access to pollinators with short mouthparts, even
if some of those pollinators might act as occasional but efficient
visitors. Plants might therefore often evolve a high degree of
evolutionary specialization despite several visitors acting as effective
pollinators due to the limited capacity to maintain pollination by a
subset of effective pollinators while precisely excluding the
ineffective ones.