Phenotypic links in complex life cycles: conclusions from studies with decapod crustaceans

Synopsis

I review studies on decapod crustaceans to draw conclusions about the importance of effects of past environmental conditions on development, phenotype, performance, and survival in animals. I consider 3 critical points of the life cycle: the allocation of reserves into eggs, the hatching of larvae, and metamorphosis from the larval to the juvenile phase. Biomass allocated to eggs varies among females as a response to changes in environmental conditions. These variations are propagated to the larval stages, influencing the biomass at hatching, subsequent larval developmental pathways, and survival during periods of limited starvation. Suboptimal conditions experienced by embryos increase the loss of mass during embryogenesis; size or biomass of the juvenile is either positively or negatively correlated with initial biomass. Positive correlations may be the normal pattern; negative correlations occur when individuals hatched with low initial biomass follow developmental pathways that lead to increased biomass at metamorphosis. In estuarine crabs, salinity experienced by embryos leads to salinity acclimation in early larval stages. Phenotypic links originate as transgenerational effects that propagate to the juvenile stages. There are least 3 types of effects: disruption of physiological processes; direct adaptive responses; and indirect consequences of adaptive mechanisms. All types appear within a species; they are produced as a response to a single environmental factor. Variability in phenotype remains latent and is expressed in terms of survival according to the environmental conditions experienced by a particular stage. The fate of individuals is thus affected by interactions between their immediate developmental processes and their environmental history.

Introduction

"You could not step twice into the same river; for other waters are ever flowing on to you. "

Eraclitus

In recent years a growing body of literature has suggested that environmental conditions may affect traits of individuals at early life phases and lead to variation in survival and reproduction of organisms with complex life cycles. This contrasts with classic attempts to explain the performance and survival of organisms as a consequence of present environmental conditions. Environmentally induced variation in traits in an early life phase (for example embryo) is carried over to the next life phase (for example larva or juvenile). In terms of survival, that variation remains latent at early stages, but is expressed later in development or at maturity. Most of the research on these phenotypic links or "carry-over effects" comes from laboratory experiments (Kunisch and Anger 1984; Pechenik and others 1998; Beckerman and others 2003; Räsänen and others 2005; Giménez and others 2004). Theoretical research also has suggested that phenotypic links lead to cohort effects, which in turn affect the dynamics of the populations through changes in the strength of density-dependence (Beckerman and others 2003). These population models differ from those using the logistic equation or stage/age structured matrix models as they consider that life-history traits may vary in time (see Beckerman and others 2002). Other theoretical consideractions suggest an important influence on connectivity among populations, settlement, and recruitment (McCormick 1998; Giménez 2003, 2004). Previous recruitment models have not considered the importance of these phenotypic links to explain recruitment limitation. Both experimental and theoretical advances call for field work evaluating the importance of natural variability in the traits of individuals and its consequences for performance. The available information suggests that phenotypic links are important to explain natural variability in survival and reproduction (Phillips 2002; Jarrett 2003; Altwegg and Reyer 2003; McCormick and Hoey 2004; Marshall and Keough 2005). Further advances may be achieved by integrating experimental and field research (Podolsky 2003).

At the present stage of development of this field it is appropriate to evaluate the existing information. Phenotypic links might have been observed for a long time but not recognized as such because they were treated as "noise," or disregarded in order to study other processes. Now such "noise" may turn out to be an interesting "signal."

Here, I review the existing data on phenotypic links that occur during the life cycle of decapod crustaceans. General characteristics of the life cycle and early development of decapod crustaceans were summarized by Anger (2001). Briefly, for the reviewed species, embryos are carried by the females for several weeks, so embryonic development occurs in the parental habitat. After hatching, larvae are released into the water with larval development usually passing through 2 or more zoeal stages plus a decapodid (= megalopa in brachyurans). Decapodids metamorphose to a first juvenile stage.

Phenotypic links in decapod crustaceans