Developmental and Evolutionary History Affect Survival in Stressful Environments

Abstract

The world is increasingly impacted by a variety of stressors that have the potential to differentially influence life history stages of organisms. Organisms have evolved to cope with some stressors, while with others they have little capacity. It is thus important to understand the effects of both developmental and evolutionary history on survival in stressful environments. We present evidence of the effects of both developmental and evolutionary history on survival of a freshwater vertebrate, the rough-skinned newt (Taricha granulosa) in an osmotically stressful environment. We compared the survival of larvae in either NaCl or MgCl2 that were exposed to salinity either as larvae only or as embryos as well. Embryonic exposure to salinity led to greater mortality of newt larvae than larval exposure alone, and this reduced survival probability was strongly linked to the carry-over effect of stunted embryonic growth in salts. Larval survival was also dependent on the type of salt (NaCl or MgCl2) the larvae were exposed to, and was lowest in MgCl2, a widely-used chemical deicer that, unlike NaCl, amphibian larvae do not have an evolutionary history of regulating at high levels. Both developmental and evolutionary history are critical factors in determining survival in this stressful environment, a pattern that may have widespread implications for the survival of animals increasingly impacted by substances with which they have little evolutionary history.

Occurrence of Amphibians in Saline Habitats: A Review and Evolutionary Perspective

“…Gadow (1901) stated that ''Common salt is poison to the Amphibia,'' and there is no doubt that amphibians are indeed osmotically challenged organisms due to their permeable skin and eggs (Shoemaker and Nagy 1977). A plethora of studies have found that salt can lead to increased mortality, developmental deformities, physiological stress, and the alteration of growth and development at (e.g., Ely 1944;Ruibal 1959;Beebee 1985;Padhye and Ghate 1992;Viertel 1999;Turtle 2000;Chinathamby et al 2006;Dougherty and Smith 2006;Collins and Russell 2009;Karraker and Ruthig 2009;Langhans et al 2009;Chambers 2011;Duff et al 2011;Harless et al 2011;Alexander et al 2012;Hopkins et al 2013a,b;Hua and Pierce 2013) and across different life-history stages (i.e., carry-over effects; Petranka and Doyle 2010;Wu et al 2012;Hopkins et al 2014). This general intolerance has been demonstrated repeatedly (and as such will not be a focus of this review) and, perhaps as a result, there are no truly marine-or salinespecialist amphibian species.…”

Effects of temperature on embryonic and early larval growth and development in the rough-skinned newt (Taricha granulosa)

“…Larvae that experienced 7°C during embryonic development did not grow as large or as developed as larvae in the other embryonic treatments, regardless of larval temperature. This inability to compensate for a "bad start" also occurs in amphibians exposed to osmotic stress during embryonic development (Hopkins et al, 2014;Wu et al, 2012). An exception to this pattern occurred at larval temperature 7°C, where larval growth (but not development) was equally slow regardless of embryonic temperature ( Fig.…”

“…These effects resulted in altered swimming performance, which has important survival implications (Watkins and Vraspir, 2006). Considering that smaller, less developed larvae are more susceptible to pollution (Beebee, 1986;Cooke, 1979;Hopkins et al, 2014) and predators (Anderson et al, 2001;Boone et al, 2002;Gall et al, 2011;Touchon et al, 2013;Warkentin, 1995), the carry-over effects of embryonic temperature in salamanders and newts could have survival consequences in later life stages.…”

“…Carry-over effects of embryonic temperature have been observed in a wide variety of taxa (reviewed by Hopkins et al (2014)), ranging from arthropods (Ernsting and Isaaks, 1997;Geister et al, 2009;Giménez, 2006) and tunicates (Thiyagarajan and Qian, 2003) to fish (Johnston et al, 1998;Martell et al, 2005Martell et al, , 2006 and reptiles (Brooks et al, 1991;Elphick and Shine, 1998;O'Steen, 1998).…”

“…Temperature has long been known to affect rates of embryonic and larval growth in these animals (Moore, 1939;Wilbur and Collins, 1973;Harkey and Semlitsch, 1988;Newman, 1989;Smith-Gill and Berven, 1979;Álvarez and Nicieza, 2002), and the discrete life stages of amphibians make them attractive models for the study of carry-over effects. Carry-over effects have been found in amphibians exposed to ultraviolet radiation (Belden and Blaustein, 2002;Pahkala et al, 2001), salinity (Wu et al, 2012;Hopkins et al, 2014), and acidic conditions (Räsänen et al, 2002), but the carry-over effects of temperature across early life-history stages are still largely unknown. Given that the world is undergoing unprecedented anthropogenic change (Steffen et al, 2007), including global climate change (IPCC, 2014), and amphibians are known to be particularly sensitive to changes in their environments (Hopkins, 2007), investigating the implications of temperature shifts on the development and growth of amphibians at and across early life-history stages is crucial for conservation efforts (Walther et al, 2002).…”