Article

Environmentally cued hatching across taxa: embryos respond to risk and opportunity.

Department of Biology, Boston University, Boston, MA 02215, USA.
Integrative and Comparative Biology (Impact Factor: 2.97). 07/2011; 51(1):14-25. DOI: 10.1093/icb/icr017
Source: PubMed

ABSTRACT Most animals begin life in eggs, protected and constrained by a capsule, shell, or other barrier. As embryos develop, their needs and abilities change, altering the costs and benefits of encapsulation, and the risks and opportunities of the outside world. When the cost/benefit ratio is better outside the egg, animals should hatch. Adaptive timing of hatching evolves in this context. However, many environmental variables affect the optimal timing of hatching so there is often no consistent best time. Across a broad range of animals, from flatworms and snails to frogs and birds, embryos hatch at different times or at different developmental stages in response to changing risks or opportunities. Embryos respond to many types of cues, assessed via different sensory modalities. Some responses appear simple. Others are surprisingly complex and sophisticated. Parents also manipulate the timing of hatching. The number and breadth of examples of cued hatching suggest that, in the absence of specific information, we should not assume that hatching timing is fixed. Our challenge now is to integrate information on the timing of hatching across taxa to better understand the diversity of patterns and how they are structured in relation to different types of environmental and developmental variation. As starting points for comparative studies, I: (1) suggest a framework based on heterokairy-individual, plastic variation in the rate, timing, or sequence of developmental events and processes-to describe patterns and mechanisms of variation in the timing of hatching; (2) briefly review the distribution of environmentally cued hatching across the three major clades of Bilateria, highlighting the diverse environmental factors and mechanisms involved; and (3) discuss factors that shape the diversity of plastic and fixed timing of hatching, drawing on evolutionary theory on phenotypic plasticity which directs our attention to fitness trade-offs, environmental heterogeneity, and predictive cues. Combining mechanistic and evolutionary perspectives is necessary because development changes organismal interactions with the environment. Integrative and comparative studies of the timing of hatching will improve our understanding of embryos as both evolving and developing organisms.

1 Follower
 · 
136 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Hatching, the life history switch point between embryonic and larval or subadult stages, has traditionally been regarded as a fixed event in an organism's development. This notion has been challenged by reports of environmentally cued hatching in recent years, which show embryos improve fitness by hatching in response to mortality risks. Here, we present evidence of accelerated hatching due to predation at two points during embryonic development in Chiromantis hansenae. Young embryos (0 day old) exposed to simulated predation hatched earlier compared to undisturbed clutches. Old embryos (4 days old) subjected to direct katydid predation had more immediate responses, hatching < 1 h after predation on average. Hatching time was not correlated with female frog size, egg attendance time, or other predator cues. Results confirm predator-cued hatching in a new family of amphibians and support hatching plasticity being a widespread and potentially ancestral condition. We suggest mechanisms and ecological basis of cue transmission and response in C. hansenae and point out potential further research.
    Behavioral Ecology and Sociobiology 09/2014; 68(11). DOI:10.1007/s00265-014-1781-0 · 3.05 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: For organisms with complex life histories it is well known that risk experienced early in life, as embryos or larvae, may have effects throughout the life cycle. Although carryover effects have been well documented in invertebrates with different levels of parental care, there are few examples of predator-induced responses in externally brooded embryos. Here, we studied the effects of nonlethal predation risk throughout the embryonic development of newly spawned eggs carried by female shrimp on the timing of egg hatching, hatchling morphology, larval development and juvenile morphology. We also determined maternal body mass at the end of the embryonic period. Exposure to predation risk cues during embryonic development led to larger larvae which also had longer rostra but reached the juvenile stage sooner, at a smaller size and with shorter rostra. There was no difference in hatching timing, but changes in larval morphology and developmental timing showed that the embryos had perceived waterborne substances indicative of predation risk. In addition to carryover effects on larval and juvenile stages, predation threat provoked a decrease of body mass in mothers exposed to predator cues while brooding. Our results suggest that risk-exposed embryos were able to recognize the same infochemicals as their mothers, manifesting a response in the free-living larval stage. Thus, future studies assessing anti-predator phenotypes should include embryonic development, which seems to determine the morphology and developmental time of subsequent life-history stages according to perceived environmental conditions.
    Zoology 04/2014; DOI:10.1016/j.zool.2013.09.004; · 1.60 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Most animals metamorphose, changing morphology, physiology, behavior and ecological interactions. Size- and habitat-dependent mortality risk is thought to affect the evolution and plastic expression of metamorphic timing, and high predation during the morphological transition is posited as a critical selective force shaping complex life cycles. Nonetheless, empirical data on how risk changes across metamorphosis and stage-specific habitats, or how that varies with size, are rare. We examined predator-prey interactions of red-eyed treefrogs, Agalychnis callidryas, with an aquatic predator (giant water bug, Belostoma) and a semi-terrestrial predator (fishing spider, Thaumasia) across metamorphosis. We manipulated tadpole density to generate variation in metamorph size and conducted predation trials at multiple developmental stages. We quantified how frog behavior (activity) changes across metamorphic development, habitats, and predator presence or absence. In aquatic trials with water bugs, frog mortality increased with forelimb emergence, as hypothesized. In semi-terrestrial trials, contrary to predictions, predation by spiders increased, not decreased, with tail resorption. In neither case did frog size affect mortality. Frogs reduced activity upon forelimb emergence in the water, and further with emergence into air, then increased activity with tail resorption. Longer-tailed metamorphs were captured more often in spider attacks, but attacked less, as most attacks followed prey movements. Metamorphs behaviorally compensated for poor escape performance more effectively on land than in water, thus emergence timing may critically affect mortality. The developmental timing of the ecological transition between environments that select for different larval and juvenile phenotypes is an important, neglected variable in studies of complex life cycles.
    Oecologia 07/2013; DOI:10.1007/s00442-013-2714-8 · 3.25 Impact Factor

Preview

Download
4 Downloads