Phylogenetic position of a bizarre lizard Harpesaurus implies the co-evolution between arboreality, locomotion, and reproductive mode in Draconinae (Squamata: Agamidae)

Abstract

Viviparous reproduction has evolved independently more than 100 times in the evolutionary history of Squamata (lizards and snakes). Adaptation to cold climates is the dominant hypothesis explaining shifts to viviparity, but viviparous species are also present in the tropical lowlands, implying the presence of other factors that may also promote the evolution of viviparity. For example, the tropical Asian/Oceanian subfamily, Draconinae, includes two viviparous genera (Cophotis and Harpesaurus). However, one of them, Harpesaurus, is extremely rare, making it difficult to study aspects of their ecology or evolution. We managed to collect a H. borneensis, and this provided an opportunity to address the evolution of viviparity in draconine lizards. Based on a new molecular phylogenetic hypothesis, including all viviparous groups in Draconinae, we infer that viviparity has evolved twice within the subfamily. Ancestral state reconstruction analyses indicated that shifts to viviparity were preceded by the evolution of arboreality and slow-moving locomotion. Our analysis strongly suggests evolutionary correlations between habitats, locomotion, and reproductive modes. Taken together, these results suggest that the use of arboreal habitats and slow locomotion facilitated the evolution of viviparity in these tropical/subtropical lizards. Arboreal, slow-moving species are considered to rely more on crypsis in predator avoidance rather than fleeing. Therefore, we propose that such species are relatively insusceptible to the concomitant cost of viviparity: reduced locomotive ability and increased risk of predation during pregnancy. We also describe and discuss the unique behaviours of H. borneensis.

Key words:

• ancestral state reconstruction
• arboreal
• deliberate locomotion
• pre-adaptation
• Sarawak
• viviparity

Acknowledgements

The State Government of Sarawak kindly permitted us to conduct the project (Permit No.NPW.907.4.4.(Jld.14)-129 and Park Permit No.66/2017) and to export biological samples (Permit No. 17568). The Research, Development, and Innovation Division, Sarawak Forest Department, provided all facilities for conducting research. We sincerely thank Haji Sapuan Bin Ahmad, Director of Forests/Controller of Wildlife/Controller of National Parks and Nature Reserves, Runi Sylvester Pungga, Paulus Meleng, and staffs at the FDS/RDID for their excellent assistance to the application of research permission. We are grateful to Stephen Antang and his staffs at Kubah National Park for kindly accepting our inventory survey in the national park. We thank Shimpei Ochi for helping fieldwork. We deeply thank two anonymous reviewers and an editor for many valuable comments and suggestions to this paper.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplemental data

Supplemental data for this article can be accessed here: https://dx.doi.org/10.1080/14772000.2020.1795741.

Associate Editor: David Gower

Additional information

Funding

This work was supported by a grant from JSPS Core-to-Core program B. Asia-Africa Science Platforms [FY2017–2019] to TK, YK, and KN (coordinator: Masaharu Motokawa, the Kyoto University Museum) and Grant-in-Aid for Early-Career Scientists to TK (# 20K15869) and by JST/JICA, SATREPS to KN (coordinator: Takao Itioka, Kyoto University). This research was also supported by the Kondo Grant of the Asahi Glass Foundation to KN and YK.