The Development of Adaptive Embryo Behavior

Trustees Of Boston University, Boston

Investigators

Abstract

Embryos of many species assess and respond to their environment in ways that matter for survival. Many features and challenges of embryonic life are broadly shared across animals, but frog eggs are particularly tractable to study. Structures such as egg capsules protect and constrain the embryo inside, creating a trade-off of costs and benefits. Upon hatching, animals enter a new environment, with both new dangers and resources. When to hatch is an essential decision embryos make, based on environmental cues. Hatching is also a physical feat that embryos must perform. The ability to assess cues, to exit the egg, and to survive outside the egg all change as embryos develop. Thus, under the same conditions, what embryos can do and what they should do to survive also changes. This project will examine how and why development changes behavior, using embryos of red-eyed treefrogs that hatch up to 40% prematurely to escape threats to the egg. It will assess the importance of maturation, adaptive changes in decisions matched to abilities, embryonic learning, and how embryos use two kinds of information; simple cues of oxygen availability and complex vibrations that can indicate predator attack. It will improve our understanding of embryo lives, behavioral development, and how animals use different kinds of information to make decisions, including broadly important but poorly understood vibrational information. The adaptive behavior of embryos is accessible and appealing, and thus ideal for scientific education and outreach. This project will offer interdisciplinary biology-engineering training for graduate and undergraduate students, as well as Neotropical research and cross-cultural experiences for US students and Latin American interns. The PIs will work with the media, museums, and zoos to disseminate results broadly. They will offer research experiences for teachers and develop online multimedia resources for educators at multiple levels. New methods and tools developed by this project will facilitate other research on embryo behavior and animal responses to vibrational cues. This project is an integrative study of the development and regulation of environmentally cued hatching in red-eyed treefrogs, for which multiple selective trade-offs shaping hatching timing are known. Embryos use cues in at least two sensory modalities for their hatching decision. Older embryos hatch more readily, but even 30%-premature embryos sometimes hatch within seconds of a cue. This project will assess: I) how the speed and success of hatching change across effector development, focusing on hatching glands; II) how sensor development changes sensitivity to cues and cue properties, addressing developmental changes in mechanoreception by the inner ear and lateral line vs. more consistent, early developed, oxygen sensing; and III) how hatching decision rules for responses to simple hypoxia cues and complex vibrational, and potentially tactile, physical disturbance cues are shaped by developmentally changing trade-offs, a history of stage-specific selection, and the earlier experiences of embryos. The team will use (a) histology and microscopy to characterize morphological changes, (b) respirometry to assess metabolic changes, (c) measures of vestibulo-ocular reflexes to assess otic function, and (d) macro-videography to analyze embryo behavior and hatching performance. They will assess ontogenetic changes in hatching under controlled hypoxia, vibration playback, and predator attacks, and develop new playback methods for separating motion and tactile components of physical disturbance cues. Mechanosensory stimuli and hypoxia are common cues for hatching across taxa. Moreover, vibrational signals and cues inform behavior in many other contexts, later in life, and oxygen availability shapes the behavior of many aquatic animals. Results from red-eyed treefrog embryos will advance our understanding of behavioral development and animal information use more broadly. Datasets will be deposited in DRYAD. Outreach materials, including images and video, will be posted on Warkentin's lab website or contributed to the Encyclopedia of Life or National Association of Biology Teachers web resource page.