Abstract Development can play a critical role in how organisms respond to changes in the environment. Tolerance to environmental challenges can vary during ontogeny, with individual- and population-level impacts that are associated with the timing of exposure relative to the timing of vulnerability. In addition, the life history consequences of different stressors can vary with the timing of exposure to stress. Salinization of freshwater ecosystems is an emerging environmental concern, and habitat salinity can change rapidly due, for example, to storm surge, runoff of road deicing salts, and rainfall. Elevated salinity can increase the demands of osmoregulation in freshwater organisms, and amphibians are particularly at risk due to their permeable skin and, in many species, semi-aquatic life cycle. In three experiments, we manipulated timing and duration of exposure to elevated salinity during larval development of southern toad (Anaxyrus terrestris) tadpoles and examined effects on survival, larval growth, and timing of and size at metamorphosis. Survival was reduced only for tadpoles exposed to elevated salinity early in development, suggesting an increase in tolerance as development proceeds; however, we found no evidence of acclimation to elevated salinity. Two forms of developmental plasticity may help to ameliorate costs of transient salinity exposure. With early salinity exposure, the return to freshwater was accompanied by a period of rapid compensatory growth, and metamorphosis ultimately occurred at a similar age and size as freshwater controls. By contrast, salinity exposure later in development led to earlier metamorphosis at reduced size, indicating an acceleration of metamorphosis as a mechanism to escape salinity stress. Thus, the consequences of transient salinity exposure were complex and were mediated by developmental state. Salinity stress experienced early in development resulted in acute costs but little long-lasting effect on survivors, while exposures later in development resulted in sublethal effects that could influence success in subsequent life stages. Overall, our results suggest that elevated salinity is more likely to affect southern toad larvae when experienced early during larval development, but even brief sublethal exposure later in development can alter life history in ways that may impact fitness.
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A novel larval diet interacts with nutritional stress to modify juvenile behaviors and glucocorticoid responses
Developmental plasticity can allow the exploitation of alternative diets. While such flexibility during early life is often adaptive, it can leave a legacy in later life that alters the overall health and fitness of an individual. Species of the spadefoot toad genus
- Award ID(s):
- 1754136
- NSF-PAR ID:
- 10449456
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 11
- Issue:
- 16
- ISSN:
- 2045-7758
- Page Range / eLocation ID:
- p. 10880-10891
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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In holometabolous insects, larval nutrition affects adult body size, a life history trait with a profound influence on performance and fitness. Individual nutritional components of larval diets are often complex and may interact with one another, necessitating the use of a geometric framework for elucidating nutritional effects. In the honey bee, Apis mellifera, nurse bees provision food to developing larvae, directly moderating growth rates and caste development. However, the eusocial nature of honey bees makes nutritional studies challenging, because diet components cannot be systematically manipulated in the hive. Using in vitro rearing, we investigated the roles and interactions between carbohydrate and protein content on larval survival, growth, and development in A. mellifera. We applied a geometric framework to determine how these two nutritional components interact across nine artificial diets. Honey bees successfully completed larval development under a wide range of protein and carbohydrate contents, with the medium protein (∼5%) diet having the highest survival. Protein and carbohydrate both had significant and non-linear effects on growth rate, with the highest growth rates observed on a medium-protein, low-carbohydrate diet. Diet composition did not have a statistically significant effect on development time. These results confirm previous findings that protein and carbohydrate content affect the growth of A. mellifera larvae. However, this study identified an interaction between carbohydrate and protein content that indicates a low-protein, high-carb diet has a negative effect on larval growth and survival. These results imply that worker recruitment in the hive would decline under low protein conditions, even when nectar abundance or honey stores are sufficient.
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Rising atmospheric CO 2 reduces seawater pH causing ocean acidification (OA). Understanding how resilient marine organisms respond to OA may help predict how community dynamics will shift as CO 2 continues rising. The common slipper shell snail Crepidula fornicata is a marine gastropod native to eastern North America that has been a successful invader along the western European coastline and elsewhere. It has also been previously shown to be resilient to global change stressors. To examine the mechanisms underlying C. fornicata’s resilience to OA, we conducted two controlled laboratory experiments. First, we examined several phenotypes and genome-wide gene expression of C. fornicata in response to pH treatments (7.5, 7.6, and 8.0) throughout the larval stage and then tested how conditions experienced as larvae influenced juvenile stages (i.e., carry-over effects). Second, we examined genome-wide gene expression patterns of C. fornicata larvae in response to acute (4, 10, 24, and 48 h) pH treatment (7.5 and 8.0). Both C. fornicata larvae and juveniles exhibited resilience to OA and their gene expression responses highlight the role of transcriptome plasticity in this resilience. Larvae did not exhibit reduced growth under OA until they were at least 8 days old. These phenotypic effects were preceded by broad transcriptomic changes, which likely served as an acclimation mechanism for combating reduced pH conditions frequently experienced in littoral zones. Larvae reared in reduced pH conditions also took longer to become competent to metamorphose. In addition, while juvenile sizes at metamorphosis reflected larval rearing pH conditions, no carry-over effects on juvenile growth rates were observed. Transcriptomic analyses suggest increased metabolism under OA, which may indicate compensation in reduced pH environments. Transcriptomic analyses through time suggest that these energetic burdens experienced under OA eventually dissipate, allowing C. fornicata to reduce metabolic demands and acclimate to reduced pH. Carry-over effects from larval OA conditions were observed in juveniles; however, these effects were larger for more severe OA conditions and larvae reared in those conditions also demonstrated less transcriptome elasticity. This study highlights the importance of assessing the effects of OA across life history stages and demonstrates how transcriptomic plasticity may allow highly resilient organisms, like C. fornicata , to acclimate to reduced pH environments.more » « less
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Many animals with complex life cycles can cope with environmental uncertainty by altering the timing of life history switch points through plasticity. Pond hydroperiod has important consequences for the fitness of aquatic organisms and many taxa alter the timing of life history switch points in response to habitat desiccation. For example, larval amphibians can metamorphose early to escape drying ponds. Such plasticity may induce variation in size and morphology of juveniles which can result in carry-over effects on jumping performance. To investigate the carry-over effects of metamorphic plasticity to pond drying, we studied the Túngara frog,
Physalaemus pustulosus , a tropical anuran that breeds in highly ephemeral habitats. We conducted an outdoor field mesocosm experiment in which we manipulated water depth and desiccation and measured time and size at metamorphosis, tibiofibula length and jumping performance. We also conducted a complimentary laboratory experiment in which we manipulated resources, water depth and desiccation. In the field experiment, metamorphs from dry-down treatments emerged earlier, but at a similar size to metamorphs from constant depth treatments. In the laboratory experiment, metamorphs from the low depth and dry-down treatments emerged earlier and smaller. In both experiments, frogs from dry-down treatments had relatively shorter legs, which negatively impacted their absolute jumping performance. In contrast, reductions in resources delayed and reduced size at metamorphosis, but had no negative effect on jumping performance. To place these results in a broader context, we review past studies on carry-over effects of the larval environment on jumping performance. Reductions in mass and limb length generally resulted in lower jumping performance across juvenile anurans tested to date. Understanding the consequences of plasticity on size, morphology and performance can elucidate the linkages between life stages. -
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Abstract Background There are a wide range of developmental strategies in animal phyla, but most insights into adult body plan formation come from direct-developing species. For indirect-developing species, there are distinct larval and adult body plans that are linked together by metamorphosis. Some outstanding questions in the development of indirect-developing organisms include the extent to which larval tissue undergoes cell death during the process of metamorphosis and when and where the tissue that will give rise to the adult originates. How do the processes of cell division and cell death redesign the body plans of indirect developers? In this study, we present patterns of cell proliferation and cell death during larval body plan development, metamorphosis, and adult body plan formation, in the hemichordate
Schizocardium californium (Cameron and Perez in Zootaxa 3569:79–88, 2012) to answer these questions.Results We identified distinct patterns of cell proliferation between larval and adult body plan formation of
S. californicum . We found that some adult tissues proliferate during the late larval phase prior to the start of overt metamorphosis. In addition, using an irradiation and transcriptomic approach, we describe a genetic signature of proliferative cells that is shared across the life history states, as well as markers that are unique to larval or juvenile states. Finally, we observed that cell death is minimal in larval stages but begins with the onset of metamorphosis.Conclusions Cell proliferation during the development of
S. californicum has distinct patterns in the formation of larval and adult body plans. However, cell death is very limited in larvae and begins during the onset of metamorphosis and into early juvenile development in specific domains. The populations of cells that proliferated and gave rise to the larvae and juveniles have a genetic signature that suggested a heterogeneous pool of proliferative progenitors, rather than a set-aside population of pluripotent cells. Taken together, we propose that the gradual morphological transformation ofS. californicum is mirrored at the cellular level and may be more representative of the development strategies that characterize metamorphosis in many metazoan animals.
