Distinguishing cophylogenetic signal from phylogenetic congruence clarifies the interplay between evolutionary history and species interactions

Interspecific interactions, including host-symbiont associations, can
profoundly affect the evolution of the interacting species. Given the
phylogenies of host and symbiont clades and knowledge of which host
species interact with which symbiont, two questions are often asked: “Do
closely related hosts interact with closely related symbionts?” and “Do
host and symbiont phylogenies mirror one another?”. These questions are
intertwined and can even collapse under specific situations, such that
they are often confused one with the other. However, in most situations, a
positive answer to the first question, hereafter referred to as
“cophylogenetic signal”, does not imply a close match between the host and
symbiont phylogenies. It suggests only that past evolutionary history has
contributed to shaping present-day interactions, which can arise, for
example, through present-day trait matching, or from a single ancient
vicariance event that increases the probability that closely related
species overlap geographically. A positive answer to the second, referred
to as “phylogenetic congruence”, is more restrictive as it suggests a
close match between the two phylogenies, which may happen, for example, if
symbiont diversification tracks host diversification or if the
diversifications of the two clades were subject to the same succession of
vicariance events. Here we apply a set of methods (ParaFit, PACo, and
eMPRess), which significance is often interpreted as evidence for
phylogenetic congruence, to simulations under three biologically realistic
scenarios of trait matching, a single ancient vicariance event, and
phylogenetic tracking. The latter is the only scenario that generates
phylogenetic congruence, whereas the first two generate a cophylogenetic
signal in the absence of phylogenetic congruence. We find that tests of
global-fit methods (ParaFit and PACo) are significant under the three
scenarios, whereas tests of event-based methods (eMPRess) are only
significant under the scenario of phylogenetic tracking. Therefore,
significant results from global-fit methods should be interpreted in terms
of cophylogenetic signal and not phylogenetic congruence; such significant
results can arise under scenarios when hosts and symbionts had independent
evolutionary histories. Conversely, significant results from event-based
methods suggest a strong form of dependency between hosts and symbionts
evolutionary histories. Clarifying the patterns detected by different
cophylogenetic methods is key to understanding how interspecific
interactions shape and are shaped by evolution.