Models of metamorphic timing: an experimental evaluation with the pond-dwelling salamander Hemidactylium scutatum (Caudata: Plethodontidae)

Abstract

Amphibian larvae vary tremendously in size at metamorphosis and length of larval period. We raised pond-dwelling four-toed salamander (Hemidactylium scutatum) larvae to test two models that predict a larva's age and size at metamorphosis. The Wilbur-Collins model proposes that the developmental rate of a larva responds to changes in growth rate in an adaptive manner throughout the larval period, and that metamorphosis can be initiated after a minimum size has been reached. The Leips-Travis or fixed-rate model states that developmental rate is set early in the larval period, perhaps by early growth rate or food availability and their positive correlation with developmental rate, and that changes in growth rate during the larval period affect size at metamorphosis, but have no effect on the age of an individual at metamorphosis. A modified version of the Wilbur-Collins model suggests that a larva's developmental rate becomes fixed about two-thirds of the way through the larval period, with changes in growth rate after that point only affecting size at metamorphosis. Larvae were raised on eight different feeding regimes which created two constant and six variable growth histories. Growth history did significantly affect size at metamorphosis. However, an a posteriori statistical test revealed a group of seven and an overlapping group of six treatments with indistinguishable lengths of larval period, indicating a general picture of a fixed developmental rate regardless of growth history. This result is unique among similar studies on invertebrates, fish, and frogs. There was no association between early growth or food level and development rates. Neither the Wilbur-Collins nor the Leips-Travis fixed-rate models were supported. The invariable developmental rate of Hemidactylium and recent osteological evidence from the literature suggest that larvae begin the process of metamorphosis as soon as they hatch, probably a trait selected for by strong predation pressure in the aquatic environment. A variety of different approaches (ecological, developmental, phylogenetic) are necessary to fully evaluate the adaptive nature of the timing of transitions between life cycle stages.

How Metamorphosis Is Different in Plethodontids: Larval Life History Perspectives on Life-Cycle Evolution

“…In their first 30 d of larval life, tadpoles can experience a 40-fold increase in mass (Beachy et al 1999; Beachy 2001), and larval ambystomatids can increase mass by 25–125 times during this period (Clarkson and Beachy 2015; Ihli and Beachy 2016). In contrast, larval plethodontids do not even double their mass during this period, even when fed ad libitum (Beachy 1995a; O’Laughlin and Harris 2000). Field observations verify the idea that larval growth is slow in plethodontids.…”

“…In addition, even in growth experiments where larval growth history is directly manipulated (e.g., Alford and Harris 1988), plethodontids fail to grow rapidly. In experiments where at least one growth treatment is to provide ad libitum food, the slowest-growing ambystomatid, Ambystoma maculatum , grows an order of magnitude faster than the fastest-growing plethodontid, Hemidactylium (Ihli and Beachy 2016; O’Laughlin and Harris 2000; Fig. 1).…”

Perspective: Embedded Molecular Switches, Anticancer Selection, and Effects on Ontogenetic Rates: A Hypothesis of Developmental Constraint on Morphogenesis and Evolution

“…The seemingly consistent relationship between larval growth rate and age at metamorphosis (ϭ1/developmental rate) provided the original data for a widely cited trade-off model for amphibian early life histories (Wilbur and Collins 1973). The model and its cousins and subsequent refinements (Alford and Harris 1988;Leips and Travis 1994;O'Laughlin and Harris 2000;Day and Rowe 2002) all suggest extrinsic control on age and size at metamorphosis via an adaptive, plastic physiological response to current environmental conditions. However, some of the more recent experiments have detected stagespecific limitations to plasticity, that is, environmental conditions early in larval development have greater effect on the age and size at metamorphosis than conditions later in larval development.…”

Life history of a small form of the plethodontid salamander Desmognathus quadramaculatus

“…Differences in larval growth rate have been shown to affect metamorphic timing in sh, frogs, ambystomatid salamanders, insects and crustaceans (Alford and Harris, 1988;Alford, 1999;Beachy et al, 1999;Harris, 1999;Hentschel, 1999;Ryan, 2000;Beachy, 2001). However, larval development and growth are decoupled in plethodontids:variation in growth rate does not result in variation in metamorphic timing (Beachy, 1995b(Beachy, , 1997O'Laughlin and Harris, 2000). Clearly, rapid larval growth can have consequences for increases in metamorphic and maturation size in plethodontids (Ryan, 1998;Camp et al, 2000), but it fails to affect metamorphic timing.…”