Evolutionary implications of hierarchical impacts of nonlethal injury on reproduction, including maternal effects

Abstract

Nonlethal injury is pervasive in metazoans, but surprisingly little is known about its impact upon reproductive allocation. The impact of injury on reproduction has been explored in some detail in lizards and salamanders, which have tails that are adapted for fat storage but are also injured or lost during predatory and social encounters. We synthesize diverse insights from these studies and propose new hypotheses using graphical models which highlight three distinct, hierarchical effects of injury on reproduction: reproductive inhibition, reduction in propagule number and diminished per-propagule investment (PPI), a maternal effect. Previous studies, which involved experimentally amputating the whole tail, have provided evidence of the first two effects, although there is little evidence of reduced PPI. We assayed these effects in free-ranging Desmognathus salamanders exhibiting naturally occurring injury. Whereas earlier studies found that tail injury prohibits reproduction (precipitating functional conflict), we found that females missing 80% of their tails, including the smallest mature individuals, still reproduce. We also detected a negative correlation between magnitude of injury and PPI, a continuous maternal effect. Continuous (graded) effects of injury on PPI have not been reported previously; neither discrete nor continuous maternal effects due to injury have been previously demonstrated in free-ranging vertebrates. The dearth of evidence for such effects may be due to the design of experimental manipulations that use all-or-nothing treatments. Future studies employing quantitative field data, or more realistic experimental treatments that mimic the continuous distribution of injury are likely to detect maternal effects arising from nonlethal injury. Although our comparative and empirical findings derive from studies of lizards and salamanders, we discuss how they apply in principle to all metazoans. Studies of these effects in nonvertebrate model systems are sorely needed.

Mercury accumulation along a contamination gradient and nondestructive indices of bioaccumulation in amphibians

“…Cardiac puncture is a recommended method for blood collection in anurans [48], and can be used repeatedly on the same individuals [49]. Although tail loss in salamander species can decrease fitness through several routes such as reduction in courtship success, locomotive performance, growth rate, or reproductive success [50], the tail is regenerated over time. Thus, the impact of tail sampling on local populations is minimized compared to the lethal alternative.…”

Peripheral injury induces long-term sensitization of defensive responses to visual and tactile stimuli in the squid Loligo pealeii, Lesueur 1821

“…Injury costs are reflected in increased predation risk (Wilson, 1992), and reduction both in growth rate (Wilbur and Semlitsch, 1990) and reproductive output (Bernardo and Agosta, 2005). Because nonlethal injuries are common and often costly and slow to repair, selection should favor individuals that can adapt their behavior and physiology for relatively long periods to compensate for injury and thereby reduce their mortality risk.…”

Caudal autotomy and regeneration in lizards

“…This strategy is used by vertebrates such as mammals (Shargal et al,'99), lizards, and amphibians (Bernardo and Agosta, 2005) as well as numerous invertebrate taxa, including echinoderms (Souter et al,'97) and crustaceans (Juanes and Smith,'95). The broad phylogenetic expression of this behavior is indicative of its high success rate and subsequent survival value.…”

“…In this review, we describe the features of this unique behavioral strategy. A recent review uses caudal autotomy in lizards and salamanders as a model system to explore the effects of non-lethal injury on repro-duction (Bernardo and Agosta, 2005). Here we provide representative examples of the phenomenon to illustrate the features of lizard tail autotomy that might be useful to explore from a neuroethological perspective.…”