Egg to juvenile period, generation time, and the evolution of larval type in marine invertebrates

Abstract

Many hypotheses have been put forward to explain the evolution of different larval types in marine invertebrates. These hypotheses have generally ignored the impact which the larval (developmental) type can have on the adult stage of the life cycle. A conceptual model presented here shows how reduction of the pre-metamorphic, or 'egg-to-juvenile' period either increases size at reproduction [by increasing the benthic (post-metamorphic) development period in the case of species with fixed duration Me cycles], or decreases overall generation times (in species with fixed size or age at reproduction, and variable life cycle duration). In either case the net result is an increase in fitness. A simple analytical version of this model is derived and is illustrated with data from 2 species of nudibranch mollusc. The model reveals an 'optimal' egg-to-juvenile period [where the intrinsic rate of increase ( K ) is maximised] for all life-cycle durations modelled. Reduction of the egg-to-juvenile period leads to an increase in r in all cases except when egg-to-juvenile period is very short. At egg-tojuvenile periods typical of species with feeding larvae, increases in r may be considerable (a reduction in egg-to-juvenile period from 100 d to 90 d yields a 4 to 13 % increase in I ) . Available evidence from several taxa indicates that developmental type and egg-to-juvenile period are correlated, such that species with non-feeding larvae tend to have shorter egg-to-juvenile periods. Consequently, the selective pressures to reduce egg-to-juvede period which are Illustrated by this model highlight a previously overlooked pressure for the evolution of non-feeding larvae in marine invertebrates.

Egg Size Evolution in Tropical American Arcid Bivalves: The Comparative Method and the Fossil Record

“…A likely ecological factor that might act in this fashion is oceanic productivity (Lessios 1990). Current models of life-history evolution in marine systems predict that egg size should be negatively correlated with productivity, because large eggs represent an increase in maternal investment per offspring that offsets the effects of low productivity and a poor feeding environment (Vance 1973;Thresher 1982;Lessios 1990;Havenhand 1995;Levitan 2000). The underlying force that drives the relationship between productivity and optimal egg size in these models is mortality.…”

“…In contrast, where high oceanic productivity provides a better larval feeding environment, selection should favor mothers who produce smaller and more numerous eggs. Because productivity regimes differ strongly between the EP and WA (D'Croz et al 1991;Wellington and Robertson 2001) and productivity has long been thought to be a major factor driving egg size evolution in marine taxa (Thorson 1950;Vance 1973;Thresher 1982;Gushing 1990;Havenhand 1995;Levitan 2000), the hypothesis that species in the WA have larger eggs than their geminates in the EP because of differences in larval feeding environment is an attractive one. There are, however, several other environmental factors that also must be considered.…”

“…Despite the tremendous body of theory surrounding the evolution of egg size in marine invertebrates (e.g., Vance 1973;Christiansen and Fenchel 1979;Strathmann 1985;Emlet et al 1987;Levitan 2000; and other studies reviewed by Havenhand 1995;McEdward 1997), there have been few direct tests of theoretical predictions. Experimental reductions in egg size have been shown to result in reduced larval size (Hart 1995;McEdward 1996), slower development through early stages (Sinervo and McEdward 1988;McEdward 1996), and decreased juvenile performance (Emlet and Hoegh-Guldberg 1997), as predicted by theory.…”

“…In general, life-history strategies of marine invertebrates are closely correlated with egg size: species that produce small eggs have high fecundity (Thorson 1950;Crisp 1976), feeding larvae with long developmental times (Thorson 1950;Strathmann 1985;Emlet et al 1987;Havenhand 1993), high dispersal and large geographic range (Bhaud 1993;Emlet 1990), and increased geological longevity (Hansen 1978(Hansen , 1980Jablonski and Lutz 1983;Jeffery and Emlet 2003), while the converse holds true for species with large eggs. In species with feeding larvae, egg size is thought to represent the action of natural selection balancing the advantages of high fecundity against the high mortality experienced by larvae that spend extended periods of time feeding in the plankton (Vance 1973;Christiansen and Fenchel 1979;Strathmann 1985;Emlet et al 1987; but see Levitan 1993).…”

“…In species with feeding larvae, egg size is thought to represent the action of natural selection balancing the advantages of high fecundity against the high mortality experienced by larvae that spend extended periods of time feeding in the plankton (Vance 1973;Christiansen and Fenchel 1979;Strathmann 1985;Emlet et al 1987; but see Levitan 1993). The evolution of large eggs and independence from larval food may also be a prerequisite for the evolutionary transition from feeding to nonfeeding development (Havenhand 1993(Havenhand , 1995Hart 1996;Hart et al 1997).…”