Coevolution of Cyanogenic Bamboos and Bamboo Lemurs on Madagascar.

Daniel J Ballhorn,Stefanie Kautz,Fanny Patrika Rakotoarivelo,Karen E Samonds

doi:10.1371/journal.pone.0158935

Abstract

Feeding strategies of specialist herbivores often originate from the coevolutionary arms race of plant defenses and counter-adaptations of herbivores. The interaction between bamboo lemurs and cyanogenic bamboos on Madagascar represents a unique system to study diffuse coevolutionary processes between mammalian herbivores and plant defenses. Bamboo lemurs have different degrees of dietary specialization while bamboos show different levels of chemical defense. In this study, we found variation in cyanogenic potential (HCNp) and nutritive characteristics among five sympatric bamboo species in the Ranomafana area, southeastern Madagascar. The HCNp ranged from 209±72 μmol cyanide*g-1 dwt in Cathariostachys madagascariensis to no cyanide in Bambusa madagascariensis. Among three sympatric bamboo lemur species, the greater bamboo lemur (Prolemur simus) has the narrowest food range as it almost exclusively feeds on the highly cyanogenic C. madagascariensis. Our data suggest that high HCNp is the derived state in bamboos. The ancestral state of lemurs is most likely "generalist" while the ancestral state of bamboo lemurs was determined as equivocal. Nevertheless, as recent bamboo lemurs comprise several "facultative specialists" and only one "obligate specialist" adaptive radiation due to increased flexibility is likely. We propose that escaping a strict food plant specialization enabled facultative specialist bamboo lemurs to inhabit diverse geographical areas.

Highlights

Antagonistic interactions between herbivores and plants, parasites and their hosts as well as predators and prey can be driven by escalating co-evolutionary arms races, in which the focus of selection on the host or prey is to escape the interaction, and the focus of selection on the enemy is to overcome those escape strategies or defenses [1,2,3]
HCNp among ground shoots of C. madagascariensis, C. capitata and N. elongatus showed no significant differences, whereas HCNp in Cephalostachyum sp. and B. madagascariensis was significantly lower (B. madagascariensis contained no detectable amounts of cyanide at all)
Branch shoots of C. madagascariensis had significantly higher cyanide concentrations compared to branch shoots of C. capitata (F = 12.33, T = 8.01, df = 30, P < 0.01)

Summary

Introduction

Antagonistic interactions between herbivores and plants, parasites and their hosts as well as predators and prey can be driven by escalating co-evolutionary arms races, in which the focus of selection on the host or prey is to escape the interaction, and the focus of selection on the enemy is to overcome those escape strategies or defenses [1,2,3]. In plant-herbivore systems, the result can be sophisticated arsenals of mechanical and chemical defenses in plants and counter-defense mechanisms ranging from behavioral to physiological adaptations in herbivores [4,5,6]. The evolution of physiological adaptations of herbivores (physiological specialists) to overcome specific toxic constituents in their host plants is commonly observed (i.e. increasing specialization), the opposite direction may evolve through the development.

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Conclusion