Poecilogony and larval ecology in the gastropod genus Alderia*

Abstract

The gastropod genus Alderia (Allman, 1845) (Opisthobranchia; Sacoglossa) contains a rare case of poecilogony, or variable larval development within a species. This paper reviews the alternative larval morphs and dispersal strategies expressed by Alderia spp., and presents new data on larval ecology, environmentally induced changes in development, and rates of metamorphosis for larvae differing in age and life history. Recent morphological and molecular analyses revealed a ciTptic poecilogonous species in the previously monotypic genus Alderia. The newly described Alderia willowi Krug et ai, 2007 occurs south of Bodega Harbor, California, and was the subject of all prior studies by Krug and co-workers. Unlike its strictly planktotrophic congener Alderia modesta (Loven, 1844), A. willowi produces either small feeding larvae that have a 30-day pre-competent period or large larvae that need not feed to metamorphose. Individuals can vary the developmental mode of their offspring, with a variable proportion switching from lecithotrophy (prevalent in summer) to planktotrophy in winter or spring; a similar shift is induced in some adults upon transfer to the laboratory. In a second dispersal polymorphism, a variable percentage of lecithotrophic larvae undergo spontaneous metamorphosis within 2 days of hatching, while their siblings disperse until induced to settle by carbohydrate cues from the host algae Vaiicheria spp. The percentage of spontaneous metamorphosis is uncorrelated with fecundity and is generally between 15-30%, a possible product of stabilizing selection on this bet-hedging dispersal strategy. Despite their different ages, competent larval morphs produced by alternative developmental pathways are similar in size, swimming behavior, and responses to dissolved settlement cues. However, competent planktotrophic larvae and older lecithotrophic larvae initiated metamorphosis faster after settlement than newly hatched lecithotrophic larvae, suggesting a link between planktonic period and habitat choice. Although rare, poecilogonous species like A. willowi offer special insights into the evolutionary causes and ecological consequences of alternative life histories.

Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

“…Similar developmental variation is found in the gastropod Alderia, where A. modesta shows only planktotrophic development, whereas A. willowi shows poecilogony; in some cases, the same individual was observed to deposit only egg masses with embryos hatching as lecithotrophic larvae just after collection, but after 20 days in captivity, 60% of the larvae from an egg mass were planktotrophic [143]. …”

Nitric oxide signaling differentially affects habitat choice by two larval morphs of the sea slugAlderia willowi: mechanistic insight into evolutionary transitions in dispersal strategies.

“…The sea slug Alderia willowi (Heterobranchia: Sacoglossa) is a specialist herbivore with bet-hedging larval strategies that provide an opportunity to investigate how signaling pathways control settlement in larvae with differing habitat requirements (Krug, 2007;Krug, 2009). Slugs produce clutches of either planktotrophic larvae, which are long-lived and feeding, or short-lived lecithotrophic larvae, which can metamorphose without feeding (Krug, 1998).…”

Not My “Type”: Larval Dispersal Dimorphisms and Bet-Hedging in Opisthobranch Life Histories

“…Individual slugs can produce planktotrophic larvae with a pelagic period exceeding one month, lecithotrophic larvae that spend hours to days in the water column, and crawl-away juveniles-in some cases, all from the same egg mass (Table 4; Krug, 1998Krug, , 2001. Poecilogony thus confers an exceptional degree of life-history flexibility and could represent a bet-hedging mechanism to cope with the unstable conditions on the estuarine mudflats where A. willowi occurs (Chia et al, 1996;Krug, 2007). It is unknown whether specimens of other poecilogonous sacoglossans such as Elysia zuleicae can similarly vary the development of their offspring, or if larval type is fixed within individuals as in Streblospio benedicti (Levin and Creed, 1986;Levin and Bridges, 1994).…”

“…Poecilogony also occurs among herbivorous sea slugs in the opisthobranch group Sacoglossa, which differ from polychaetes in several key respects (Krug, 2007). Sacoglossans are specialized herbivores that feed on coenocytic algae, with most species restricted to one algal genus (Jensen, 1997).…”

“…Slugs depend on spatially patchy resources that fluctuate markedly over time, which could favor bethedging strategies (Clark, 1975;Clark and DeFreese, 1987;Trowbridge, 1992Trowbridge, , 1993Trowbridge, , 2002. Embryos develop inside benthic egg masses; planktotrophic larvae settle after an extended planktonic period, whereas lecithotrophic larvae metamorphose (a) after hatching, if cues from host algae are present; (b) after hatching, with no inductive requirement; or (c) prior to hatching (intracapsular metamorphosis) (Krug, 2007). The Pacific species Alderia willowi expresses all four of those dispersal strategies, and individual adults can vary larval type among and within clutches (Krug, 1998(Krug, , 2001Smolensky et al, 2009).…”