EVOLUTIONARY LOSS OF LARVAL FEEDING: DEVELOPMENT, FORM AND FUNCTION IN A FACULTATIVELY FEEDING LARVA, BRISASTER LATIFRONS

Abstract

Species with large eggs and nonfeeding larvae have evolved many times from ancestors with smaller eggs and feeding larvae in numerous groups of aquatic invertebrates and amphibians. This change in reproductive allocation and larval form is often accompanied by dramatic changes in development. Little is known of this transformation because the intermediate form (a facultatively feeding larva) is rare. Knowledge of facultatively feeding larvae may help explain the conditions under which nonfeeding larvae evolve. Two hypotheses concerning the evolutionary loss of larval feeding are as follows: (1) large eggs evolve before modifications in larval development, and (2) the intermediate form (facultatively feeding larva) is evolutionarily short-lived. I show that larvae of a heart urchin, Brisaster latifrons, are capable of feeding but do not require food to complete larval development. Food for larvae appears to have little effect on larval growth and development. The development, form, and suspension feeding mechanism of these larvae are similar to those of obligate-feeding larvae of other echinoids. Feeding rates of Brisaster larvae are similar to cooccurring, obligate-feeding echinoid larvae but are low relative to the large size of Brisaster larvae. The comparison shows that in Brisaster large egg size, independence from larval food, and relatively low feeding rate have evolved before the heterochronies and modified developmental mechanisms common in nonfeeding echinoid larvae. If it is general, the result suggests that hypotheses concerning the origin of nonfeeding larval development should be based on ecological factors that affect natural selection for large eggs, rather than on the evolution of heterochronies and developmental novelties in particular clades. I also discuss alternative hypotheses concerning the evolutionary persistence of facultative larval feeding as a reproductive strategy. These hypotheses could be tested against a phylogenetic hypothesis.

Some Limitations of Ancestral Character-State Reconstruction When Testing Evolutionary Hypotheses

“…He identi ed an ordered series for three classes of larvae: obligate feeding ® facultative feeding ® nonfeeding. Using arguments similar to Strathmann's, Wray argued that obligate feeding is the primitive condition and has been replaced in many lineages by facultative feeding and nonfeeding (see also Emlet, 1986;Hart, 1996). Facultative feeders have very large egg yolks, and although they are able to feed, can undergo metamorphosis without feeding (Emlet, 1986;Wray and Raff, 1991;Hart, 1996).…”

The Assumptions and Challenges of Ancestral State Reconstructions

“…Many character states in diverse groups of organisms have long been thought to be more easily lost than gained (Dollo, 1893;Simpson, 1953), e.g., feeding larvae in marine invertebrates (Strathmann, 1978;Hart, 1996;Cunningham, 1999), wings in insects (Maddison, 1994), and functional wings in birds (Livezey, 1989). Most of these are complex character states that the authors argued could be lost repeatedly, but once lost, could not be regained easily.…”

Intermediate modes of larval development: bridging the gap between planktotrophy and lecithotrophy

“…We suggest the use of the term ''facultative feeding,'' rather than the more common ''facultative planktotrophy'' because it can be applied to a greater diversity of larval forms. Facultative planktotrophs are a subset of facultative feeders that obtain exogenous food from planktonic sources (e.g., Emlet 1986;Hart 1996). This is in contrast to those facultative feeders that obtain exogenous food from benthic sources (e.g., benthic detritivores).…”