Hyper-specialized bamboo lemurs possess a reduced suite of xenobiotic-metabolizing cytochrome P450 genes

Subfamilies of cytochrome P450 proteins have been strongly linked to the
metabolism of physiologically disruptive compounds such as alkaloids,
terpenoids, and other xenobiotics. Consistent with this function, these
genes have adaptively evolved in response to environmental pressures
exerted on animals, such as herbivores, that consume elevated amounts of
toxic xenobiotics or plant secondary metabolites (PSMs). Theory on
evolutionary tradeoffs predicts that highly specialized herbivores should
exhibit a relatively narrow toolkit of adaptations to accommodate the
concomitantly narrow arrays of PSMs in their diets. The bamboo lemurs of
Madagascar (genera Prolemur and Hapalemur) represent an interesting test
case for this theory because of their dietary hyper-specialization, as
these lemurs consume bamboo and grasses at rates otherwise unseen in the
order Primates. To test whether the hyper-specialized folivory of these
primates is reflected in a similarly specialized and narrow P450 gene
suite, we assembled a dataset of confidently assembled CYP1-3 genes for
two species of bamboo lemur and 13 additional lemur species. With this
dataset, we tested the predictions that bamboo lemurs would exhibit,
first, greater rates of gene loss for xenobiotic-metabolizing P450s and,
second, relaxed selection on xenobiotic-metabolizing P450 subfamilies
relative to lemurs without such dietary hyper-specialization. We found
support for the prediction of gene loss in the CYP2B, CYP2C, CYP2D, CYP2J,
and CYP3A subfamilies, all of which encode xenobiotic metabolizers. We
inferred relaxation of selection for the CYP1A and CYP2D subfamilies. The
CYP2F subfamily exhibited a signal of significant intensification of
selection in the bamboo-lemur lineage. The evolution of the P450 genes in
bamboo lemurs provides support for the evolutionary tradeoff hypothesis,
and we further hypothesize that, rather than adapting to a general array
of PSMs, bamboo lemurs have instead adapted to the primary toxin in their
diet, the highly potent poison cyanide.