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: 2.93). 07/2011; 51(1):14-25. DOI: 10.1093/icb/icr017
Source: PubMed


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.

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    • "Many studies suggest that hatching may be plastic more often than previously known or assumed (Warkentin 2011a). If hatching is plastic, individuals may improve their survival by altering hatching time (Warkentin 2011a). For example, hatching can be a way for embryos, which are relatively immobile, to escape predation (Warkentin 1995, 2000; Saenz et al. 2003; Strathmann et al. 2010). "
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    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 · 2.35 Impact Factor
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    • "The sort of plastic responses to environmental variation we document here are being increasingly found across the Bilateria [50] and are likely pervasive in nature. Furthermore, these responses early in the life of an animal can have unexpected lasting effects. "
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    ABSTRACT: Many animals respond to predation risk by altering their morphology, behavior, or life-history. We know a great deal about the cues prey respond to and the changes to prey that can be induced by predation risk, but less is known about how plastic responses to predators may be affected by separate plastic responses occurring earlier in life, particularly during the embryonic period. Embryos of a broad array of taxa can respond to egg- or larval-stage risks by altering hatching timing, which may alter the way organisms respond to future predators. Using the red-eyed treefrog (Agalychnis callidryas), a model for understanding the effects of plasticity across life-stages, we assessed how the combined effects of induced variation in the timing of embryo hatching and variation in the larval predator community impacted tadpole morphology, pigmentation and swimming performance. We found that A. callidryas tadpoles developed deeper tail muscles and fins and darker pigmentation in response to fish predators, either when alone or in diverse community with other predators. Tadpoles altered morphology much less so to dragonfly naiads or water bugs. Interestingly, morphological responses to predators were also affected by induced differences in hatching age, with early and late-hatched tadpoles exhibiting different allometric relationships between tail height and body length in different predator environments. Beyond induced morphological changes, fish predators often damaged tadpoles' tails without killing them (i.e., sublethal predation), but these tadpoles swam equally quickly to those with fully intact tails. This was due to the fact that tadpoles with more damaged tails increased tail beats to achieve equal swimming speed. This study demonstrates that plastic phenotypic responses to predation risk can be influenced by a complex combination of responses to both the embryo and larval environments, but also that prey performance can be highly resilient to sublethal predation.
    PLoS ONE 06/2014; 9(6):e100623. DOI:10.1371/journal.pone.0100623 · 3.23 Impact Factor
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    • "For instance, embryonic exposure to egg predators may favor early hatching at a smaller size and less developed stage. Such effects have been widely demonstrated in amphibians, the best-studied taxa with regard to predator-induced hatching plasticity (Warkentin, 2011; Touchon et al., 2013). Plasticity in hatching can also adjust risks of benthic and planktonic development in benthic marine invertebrates. "
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    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; · 1.67 Impact Factor
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