DISCUSSION
For a deeper understanding of the potential coevolution between lemur
and plants, we tested for cophylogenetic signals in plant-lemur
interactions, and detected significant, although weak, signals in
frugivory, folivory, florivory and granivory interactions. In the case
of frugivory, plant speciation seems to have influenced lemur body size,
at the same time that lemur speciation modulated diaspore size. Weak
cophylogenetic signals do not necessarily imply lack of evolutionary
history shared between symbiotic partners. Indeed, cophylogenetic
patterns observed for frugivory, florivory and granivory emerged from
lemurs sharing similar sets of partners interacting with
phylogenetically-related plants with no reciprocal trend. In the case of
folivory, plant diversification was also affected by lemurs. Our results
do not give support to a strong coevolutionary diversification between
lemurs and plants, in agreement with previous observations for
Neotropical primates and Angiosperms (Fuzessy et al. 2022). Instead, our
findings reflect that lemur feeding behavior is very generalist,
specially of large lemur species, and support the idea that
cophylogenetic signals are modulated by processes that are not directly
related to strong co-speciation events, such as vicariance, phylogenetic
tracking, and diffuse coevolution (Blasco-Costa el al. 2021).
The role of vicariance in coevolution —where common biogeographic
events cause subdivision of distribution ranges of interacting partners
—is dependent on the geographic scale. Vicariance contributes to
coevolutionary processes by promoting diversification of entire
populations that become isolated from each other. Over time, as
populations diverge and adapt to their respective environments and
evolve distinct and specialized structures and traits, including those
that are important for their close relationship, they become less
compatible. In this sense, vicariance is associated with high
cophylogenetic signals (Blasco-Costa el al. 2021), so in the specific
case of Madagascar, especially in the context of a relatively small
island, it is not expected to play a significant role. Phylogenetic
tracking is also usually associated with high cophylogenetic signals. It
refers to a tendency of interacting partners to track each other’s
evolutionary history, such that closely related species are more likely
to interact than distantly related species (Blasco-Costa et al. 2021).
Despite our finding of low cophylogenetic signals in lemur-plant
interactions, phylogenetic congruence arose even in a supergeneralist
system where other plant-consuming animals, such as insects and other
vertebrates, may also be shaping plant diversification. The patterns
observed here for frugivory, florivory and granivory emerged from
similar lemurs interacting with closely related plants with no
reciprocal trend (i.e., plant diversification was unaffected by lemurs).
In this case, generalist lemurs seem to be tracking temporal
fluctuations in resource availability, and increasing the consumption of
one plant species at the expense of decreased consumption of an
alternative, phylogenetically-related, resource, known as switching
behavior (Carnicer et al. 2008). Such low levels of CS associated with a
correlation between phylogenetic distances and dissimilarities in sets
of interacting plants for lemurs can be interpreted as an indicative
case of diffuse coevolution. In this sense, each lemur species interacts
with a set of plants, and experiences a complex suite of selective
pressures derived from the set of plant species they interact with.
In the case of folivory, similar plants were also found to interact with
closely related lemur species, as an indicative of coevolution. Except
for the strict folivorous genera Hapalemur and Lepilemur ,
lemurs use a variety of resources as feeding items, such as fruits,
leaves flowers, seeds, nuts, nectar, and animal prey. Regardless of the
main resource, leaves constitute an important resource for most species,
reinforcing the idea that lemur-plant interactions are quite generalist.
A weak cophylogenetic signals associated with positive correlations
between phylogenetic distances and dissimilarities in sets of
interacting partners for both lemurs and plants may also be interpreted
as a case of diffuse coevolution, since distinct amounts of each feeding
item vary across taxa, and other coexisting frugivorous and herbivorous
clades act together, thus, favoring a diffuse coevolutionary process
(Erikson 2016).
The multi-specific nature of the process delineating cophylogenetic
patterns, as observed here, does not necessarily mean either that lemurs
and plants have not coevolved, or that coevolution has necessarily been
the primary force fueling diversification (e.g. Althoff et al. 2014;
Fuzessy et al. 2022). Taken together, our results agree with the notion
that vertebrates and plants can influence each other evolution but also
highlight that they do not share a very tight coevolutionary history
(Valenta & Nevo 2020, Fuzessy at al. 2022), such as those observed in
host-parasite interactions (Gandon & Michalakis 2002) or in some
plant-pollinator systems (Herrera 2019). Spatio-temporal asymmetries,
disruptions in the strength of the relationships between interacting
partners, and shifts between periods of coevolution and independent
evolution seem to be leading to adaptive changes, ultimately resulting
in a weak and continuous process (Erikson 2016), in agreement with
previous observations in the Neotropics (Fuzessy et al. 2022). The
resemblance between Madagascar and the Neotropics is remarkable, given
that the number of frugivorous mammals in Madagascar is low when
compared to other tropical communities, which are dominated for
frugivorous primates (Fleming et al. 1987; Goodman & Ganzhorn 1997). In
Madagascar, there are very few medium-sized strictly frugivorous lemurs
(mostly Varecia and some species of Eulemur ), and the
proportion of fruits consumed by Malagasy lemurs is low compared with
primates in other regions (Fleagle & Reed 1996). The distinctive
phenology of Malagasy forests, associated with a great variability in
spatio-temporal fruit availability has been proposed as the main drivers
of the underrepresentation of frugivores in Madagascar (Dewar & Richar
2007). These patterns highlight potential risks associated with the
current disruption of lemur-plant interactions. Despite high levels of
generalism, we have shown that extant lemur-plant interactions are
phylogenetically constrained, so if a species belonging to an already
limited community of frugivores is lost, the probability of other
species to fulfill the vacant role is reduced. This issue may be
exacerbated if the species lost play the role of both dispersers and
pollinators, as is the case between the black-and-white ruffed lemur,Varecia variegata , and the traveler palm, Ravenala
madagascariensis (Kress et al. 1994). Such double mutualisms appear to
be highly prevalent in island ecosystems, and pose additional risks for
the continuing health of these forests when facing the extinction of
frugivorous animal partners (Fuster et al. 2019).
Overall, lemurs consumed plant species that were more closely related
than expected by chance, potentially indicating the consumption of
plants with similar traits. In addition, invasive plant species have not
disrupted the cophylogenetic structure of the interaction networks,
suggesting a deep conservatism of interactions (or a low invasion rate
in Madagascar). Indeed, we found no clear pattern of the influence of
plant traits on the cophylogenetic signals. Nevertheless, to make any
precise statement in this regard, we need complete and more detailed
information on plant traits, including those related to fruits, leaves,
and flowers, which are most frequently consumed by lemurs. Therefore, we
encourage future studies to characterize Malagasy flora in terms of
functional characteristics related to interactions with mutualistic and
antagonistic partners (e. g. Albert-Daviaud et al. 2021).
Lemur feeding preferences and activity patterns likely shaped the
congruence between their phylogeny with that of plants. Due to the
unique ecology of Madagascar, lemurs evolved to occupy a wide range of
niches, from night-living arboreal insectivores to ground-dwelling
cathemeral folivores-frugivores, and diurnal frugivores (Gould &
Sauther 2006). As expected, nocturnal lemurs and those that include a
great amount of insects in their diets (and the least amount of plants),
showed the largest Procrustean residuals, and contributed the least to
the shared evolutionary history with plants, regardless of interaction
type, and in agreement with previous studies (Fuzessy et al. 2022).
Overall, diet and activity patterns have been important drivers of lemur
evolution, shaping morphology, physiology, and behavior in unique ways
that have allowed them to thrive in Malagasy diverse habitats. Dietary
adaptations have driven the evolution of morphological and physiological
features, such as specialized teeth, tongue, digestive systems, and
metabolic rates (Cuozzo & Yamashita 2006; Powzyk & Mowry 2006; Pastor
et al. 2021). Over evolutionary time, insectivores such asDaubetonia , for instance, have evolved specialized teeth and long
fingers that are adapted for catching and handling prey, added to an
enhanced night vision and specialized auditory systems to aid in hunting
(Goodman et al. 1993; Sterling & McCreless 2006; Lhota et al. 2008). On
the other hand, lemurs that consume great amounts of fruits and flowers
have evolved color vision to help them distinguish ripe fruits and
identify flowers, specially from a conspicuous background (Nevo et al.
2018).
Our study highlighted the important role of evolutionary history in
structuring modern interaction patterns between vertebrates and plants.
Our cophylogenetic analysis compared phylogenies of interacting partners
based on observed extant interactions presented as binary lemur-plant
interaction matrices. While this approach provides an important basis
for investigating cophylogenetic relationships (Balbuena et al. 2013;
Blasco-Costa et al. 2021), it ignores that the strength of associations
among interacting partners may affect evolutionary outcomes, and thus
precludes a deeper assessment of cophylogenetic processes. In the case
of frugivory interactions, in addition to the congruence between plant
and lemur phylogenies, we also detected a congruence between lemur
phylogeny and plant morphology, and between plant phylogeny and lemur
morphology. Although this result suggests that, to some extent, plant
speciation shaped lemur body size, and lemur speciation somehow affected
diaspore morphology, we still lack sufficient information on the role of
plant traits, including those related to fruits, leaves, and flowers, in
shaping the cophylogenetic patterns described. Studies characterizing
Malagasy flora in terms of functional characteristics related to
interactions with mutualistic and antagonistic partners are urgently
required (e. g. Albert-Daviaud et al. 2021). Despite these limitations,
results presented here shed unprecedented light on the potential for
supergeneralist interactions, including both antagonisms and mutualisms,
to shape shared evolutionary trajectories between vertebrates and
Angiosperms.