Introduction
The divergence of functional traits is usually influenced by multiple
factors, and disentangling the relative contributions of these factors
is important for understanding the evolutionary drivers of traits.
Fruit type is a fundamental trait in
plant biology, as it is a key component for seed dispersal, thereby
linking reproduction of individual plants to regeneration of ecological
communities (Howe & Smallwood 1982; Jordano et al. 2007; Seale
& Nakayama 2020). Fruits can be dichotomously classified as fleshy or
dry. The composition of fleshy versus dry fruits varies greatly across
communities and climate regions, with an increasing proportion of
fleshy-fruited species occurring
with both decreasing latitude and altitude at a global scale (Willsonet al. 1989; Almeida-Neto et al. 2008; Chen et al.2017; Albert et al. 2018; Zhao et al. 2018). Although many
factors have been proposed to explain this pattern, the relative
importance of each factor has not yet been resolved. Here, we analyze a
very large dataset to disentangle the relative contributions to the
variation in fruit type of three factors that are most often included as
possible explanations for fleshy versus dry fruits: plant growth form,
environmental/climate factors (as summarized by the climate region in
which species occur), and phylogenetic conservatism (evolutionary
history).
Spatial variation in climate mediates the latitudinal and altitudinal
patterns in functional traits of plants (Reich & Oleksyn 2004; Moleset al. 2007; Diaz et al. 2016). In general, precipitation
is positively associated with the proportion of fleshy fruits (Correaet al. 2015; Chen et al. 2017; Zhao et al. 2018),
as water availability is a crucial factor for the development of fleshy
fruits (Coombe 1976). High temperature is also associated with an
increasing proportion of species producing fleshy fruits (Willsonet al. 1989; Zhao et al. 2018), possibly because succulent
fleshy fruits cannot survive freezing conditions (Burke et al.1976). By analyzing the effect of 15 climatic variables on the
latitudinal pattern in fruit types of 4008 Australian species, Chenet al. (2017) showed that wet, warm, and stable climates
predicted a higher proportion of fleshy-fruited species. Furthermore,
frugivory may be another possible explanation, as tropics usually hold
more species and greater abundance of fruit-eating animals than
temperate regions (Kissling et al. 2009; Onstein et al.2017).
Plant growth form is often a predictor of other functional traits, for
example, seed mass, stem specific density, and leaf area (Moles et
al. 2005; Diaz et al. 2016). Fruit type is also strongly related
to plant growth form, showing that trees and shrubs are more likely to
produce fleshy fruits, while herbs are more likely to produce dry fruits
(Chen et al. 2004; Bolmgren & Eriksson 2005; Cortes-Floreset al. 2013). de Queiroz (2002) proposed that the cost of
producing fleshy fruits may reduce seed output, which would have
proportionally more negative effects on small and short-lived plants.
Furthermore, in the context of apparency theory (Feeny 1976), large and
long-lived woody species that produce fleshy fruits may better advertise
to frugivores than herbaceous fleshy species. Using a global dataset,
Moles et al. (2009) showed a remarkable relationship between
latitude and plant height, indicating that more trees occurred in the
tropics than in the temperate regions. In this way, the latitudinal
gradient in fruit type could be a reflection of the latitudinal gradient
in growth form.
Phylogenetic signal of specific functional traits may be a consequence
of either adaptation among phylogenetically related species that share
similar environments or phylogenetic conservatism (Blomberg et
al. 2003). Although the shift between fleshy and dry fruit occurred
independently in many plant lineages as a response to environmental
filters (Bolmgren & Eriksson 2005), a significant phylogenetic signal
can still be detected (Herrera 2002; Chen et al. 2017),
indicating that phylogenetic conservatism is a potential factor
explaining fruit type. We therefore may expect the different composition
of fruit types among floras to reflect their evolutionary histories.
Furthermore, plant growth form may be also phylogenetically controlled,
as are many other plant functional traits such as seed mass (Moleset al. 2005), leaf traits (Pearse & Hipp 2009) and root traits
(Valverde-Barrantes et al. 2017). Therefore, we further expected
that the phylogenetic conservatism might play an important role in
determining the divergence of fruit type.
In
summary, plant growth form, climatic factors, and phylogenetic
conservatism may account, at least in part, for the pattern of fleshy
versus dry fruit types (Bolmgren & Eriksson 2005; Cortes-Floreset al. 2013; Chen et al. 2017). However, disentangling the
relative contributions of each factor is a challenge. Two common methods
have been performed to partition variance of a target functional trait
among possible predictor variables.
Phylogenetic generalized least
squares models (PGLS) with the phylogenetic tree treated as the error
covariance structure can be used to compare the relative contributions
among predictor variables after accounting for phylogenetic
non-independence of species; however, PGLS models do not directly give a
way to partition sources of variation explaining a trait. Nested ANOVAs
and linear mixed models with several taxonomical levels (e.g., order,
family, and genus) treated as nested random effects can be used to
disentangle the relative contributions among multiple predictors,
including phylogeny (Chen et al. 2004; Valverde-Barranteset al. 2017). However, these models only consider the nested
hierarchy of a few taxonomical levels, which oversimplifies the
phylogeny of related taxa. Furthermore, interpreting the partition of
contributions of multiple factors to the total explained variance
(R2) in the linear mixed model may be confounded when
there is correlation between predictor variables (e.g., latitude and
growth form). Therefore, to assess the roles of plant growth form,
climate region, and phylogenetic conservatism on whether species produce
fleshy or dry fruit, we used a phylogenetic partial R2that measures the reduction of explained variance when each factor is
removed from a full model containing all other predictors (Ives & Li
2018; Ives 2019). Thus, the partial R2 values give the
amount of variation explained by a predictor by asking how much of the
explained variation is lost when the factor is removed.
In this study,
we
give a quantitative analysis of the relative contributions of plant
growth form, climate region, and phylogenetic conservatism to the
variation of fruit type with a data set including 9,370 species from
Southwest China which represent a tropical, subtropical, and temperate
flora.
We
predicted that (i) woody species produce more fleshy fruits than herbs;
(ii) more fleshy-fruit species occur in tropical than in subtropical and
temperate floras climate regions; and (iii) fruit type is
phylogenetically conserved. Because we found that phylogenetic
conservativism in fruit type was extremely strong, we further
investigated whether this was due to ancient or recent phylogenetic
relationships towards the base or tips of the phylogeny, respectively.
Finally, we investigated the phylogenetic conservatism of climate region
and plant growth form: if fruit type were to show greater phylogenetic
conservatism than either of these predictor variables, then it would not
be surprising that they are poor predictors, because the greater
phylogenetic conservatism of fruit type would limit its evolutionary
response to the predictors.