Stress Hormones and the Fitness Consequences Associated with the Transition to a Novel Diet in Larval Amphibians
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3743 The Journal of Experimental Biology 212, 3743-3750 Published by The Company of Biologists 2009 doi:10.1242/jeb.034066 Stress hormones and the fitness consequences associated with the transition to a novel diet in larval amphibians Cris C. Ledón-Rettig1,*, David W. Pfennig1 and Erica J. Crespi2 1Department of Biology, University of North Carolina, CB#3280, Coker Hall, Chapel Hill, NC 27599, USA and 2Department of Biology, Vassar College, 124 Raymond Ave. Box 731, Poughkeepsie, NY 12604, USA *Author for correspondence ([email protected]) Accepted 10 August 2009 SUMMARY Closely related species often specialize on different types of prey, but little is known about the fitness consequences of making an evolutionary transition to a novel diet. Spadefoot toad larvae provide a unique opportunity to reconstruct these evolutionary events. Although most anuran larvae feed on detritus or plankton, Spea larvae have also evolved the ability to consume large anostracan fairy shrimp. To investigate the changes that may have accompanied the shift to shrimp prey, we compared shrimp- induced physiological responses of Spea larvae with those of its sister genus, Scaphiopus, that has not made this transition. Although Spea larvae performed equally well on either diet, shrimp-fed Scaphiopus larvae experienced reduced growth and developmental rates, as well as elevated levels of the stress hormone corticosterone when compared with those that ate the ancestral detritus diet. These results suggest that ancestral Spea likely experienced reduced fitness when they first adopted a carnivorous feeding strategy. Key words: corticosterone, novelty, predation, anuran larvae, food restriction INTRODUCTION is likely the ancestral diet of anuran larvae (Altig et al., 2007). Evolutionary diversification in animals is often accompanied by a According to character state reconstruction analysis, Spea is the only change in resource use (Simpson, 1953; Schluter, 2000; Grant and genus within the Pelobatoidea that has evolved the ability to exploit Grant, 2008). For example, closely related, sympatric species macroscopic prey (Ledón-Rettig et al., 2008). The evolution of typically differ in the prey on which they specialize, presumably as carnivory in these tadpoles is associated with reduced intra- and an evolutionary response that minimizes interspecific competition inter-specific competition for food (Pfennig, 1992; Pfennig et al., (reviewed by Schluter, 2000). Yet, such species must have had 2007; Martin and Pfennig, 2009). Although this ecological scenario similar dietary preferences before they diverged, suggesting that suggests potential fitness benefits to be gained from a carnivorous shifts in resource use often accompany diversification. Despite the diet, especially when resources are limited, multiple characteristics importance of dietary shifts, little is known about the physiological are needed to sense, obtain, digest and assimilate nutrients from changes and fitness consequences that accompany them. such prey. In order to better understand how ancestral populations One way to assess the consequences of dietary transitions is to of Spea may have shifted to a carnivorous diet, we examined the compare diet-induced responses in species or populations that exhibit physiological changes that occur when larvae of Scaphiopus couchii an ancestral feeding strategy relative to those that have undergone Cope, a detritivore species in Speas sister genus (García-Paris et a transition to a novel diet. Some studies that have taken this al., 2003), consume anostracan shrimp, a common prey item of approach have found that populations may initially suffer a fitness modern Spea larvae (Pfennig, 1992; Pomeroy, 1981). cost as they make this transition. For example, Phillips and Shine We hypothesize that the transition to a carnivorous diet in (Phillips and Shine, 2006) found that when black snakes from spadefoot tadpoles may have been associated with the inability of Australia first encountered a novel prey item (introduced cane toads) tadpoles to ingest or acquire nutrients from such a diet, thus causing the snakes probably suffered reduced fitness (cane toads are toxic). nutrient stress that can have negative fitness consequences. Food Black snakes were only able to prey consistently on cane toads once restriction generates substantial morphological and developmental they had evolved behavioral and physiological traits that enabled plasticity among anuran (Wilbur and Collins, 1973; Werner and them to cope with such prey. Furthermore, when organisms are Anholt, 1996; Kupferberg, 1997) and urodele (Wildy et al., 2001; presented with novel dietary resources, they may lack the behavioral, Rohr et al., 2004) larvae. Generally, studies have shown that food physiological or morphological characteristics for consuming that restriction causes reduced body sizes at metamorphosis, but the diet; thus a food-restricted condition either as a result of the inability effects on development time vary depending on when the restriction to capture prey items or extract nutrients from prey items once is experienced. During early developmental stages food restriction ingested may be costly (e.g. Carroll et al., 1998). Whether such extends larval periods, as a minimum body size needs to be reached fitness costs are generally associated with dietary transitions is before metamorphosis can occur (Wilbur and Collins, 1973). By unclear. contrast, food restriction experienced during later developmental We investigated the physiological changes associated with the stages accelerates metamorphic timing [in spadefoots (Newman, transition to a novel diet in spadefoot toad larvae (Pelobatoidea). 1987; Morey and Reznick, 2004)]. Spadefoot toads typically develop Most species within the Pelobatoidea clade feed on detritus, which in short-lived ephemeral ponds that not only vary in initial resource 4(% */52.!, /& %80%2)-%.4!, ")/,/'9 3744 C. C. Ledón-Rettig, D. W. Pfennig and E. J. Crespi abundance, but also become depleted in resources as they dry bombifrons population particularly carnivorous (Pfennig and (Pfennig, 1990; Pfennig et al., 1991). Given that growth and Murphy, 2000; Pfennig and Murphy, 2002; Pfennig et al., 2007). developmental rate are both under strong, positive, directional Despite the recurrence of shrimp from year to year in this area, selection in spadefoots, reduced growth and development caused Scaphiopus couchii feeds solely on detritus and microorganisms, by nutrient restriction probably represents a fitness cost. although they will consume shrimp in the lab if it is the only available Physiologically, this plasticity in developmental timing and size resource (Ledón-Rettig et al., 2008). Captured animals had been at metamorphosis in response to food restriction (or other housed in a colony at the University of North Carolina, Chapel Hill environmental stressors) is predominantly controlled by the for 12years. To induce breeding, male and female adults were neuroendocrine stress axis (reviewed by Denver, 2009). Recent injected with 0.07ml luteinizing hormone-releasing hormone (Sigma studies in anuran tadpoles have shown that the stress axis is activated L-7134, St Louis, MO, USA) and left for 8h in nursery tanks. All in response to food restriction (Crespi and Denver, 2005) or procedures were carried out in compliance with the Institutional increased competition for food (Glennemeier and Denver, 2002a), Animal Care and Use Committee at the University of North resulting in increased corticosterone (CORT) content (the primary Carolina, Chapel Hill, under application # 03-0110. glucocorticoid in tadpoles), increased thyroid hormone secretion and accelerated development rates (Denver, 2009). Elevated CORT Effects of diet on growth, development and whole-body CORT during food restriction has been observed in other vertebrates, and One sibship each of Sp. bombifrons and Sc. couchii were bred for acts to inhibit growth while increasing gluconeogenesis and this experiment. After hatching (3days after breeding), larvae from mobilizing energy stores from protein or lipid stores, to yield the each sibship were transferred to individual 3oz (~84g) plastic cups, necessary energetic resources needed to forage or seek more assigned a particular treatment, and then randomized and favorable conditions in the absence of nutrient inputs (Denver et interspersed on racks in the same room maintained at 26°C and on al., 2002; McEwen and Wingfield, 2003). a 14h:10h L:D photoperiod. In most anuran larvae feeding is In terms of diet transitions, the stress response to a novel diet precluded in early development by a plug of endoderm in the could invoke morphological and physiological plasticity [i.e. cryptic esophageal region (Wright, 2005). This plug is cleared in spadefoot phenotypic variation (Queitsch et al., 2002)] that facilitates the larvae only after hatching, thus no food was administered during digestion of the novel food item. In spadefoot toads, for example, the first 3days of development. On day4 after breeding, larvae were intestines of Sc. couchii tadpoles exposed to a novel shrimp diet fed either brine shrimp nauplii, ground fish food (hereafter, detritus), shorten to look more like the guts of carnivorous tadpoles (Ledón- or received no food; brine shrimp resemble the fairy shrimp that Rettig et al., 2008), thus sparing developmental resources that would Spea feed on in nature, whereas ground fish food resembles detritus otherwise be squandered on an unemployed organ (Diamond,