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Phenotypic Plasticity of Feeding Structures in Marine Invertebrate Larvae CHAPTER 8 Phenotypic Plasticity of Feeding Structures in Marine Invertebrate Larvae Justin S. McAlister and Benjamin G. Miner Researchers have worked over the last thirty years Scheiner (2004). Here we summarize some of the to examine and understand phenotypic plasticity main concepts in order to facilitate discussion of in larvae of marine invertebrates. These studies plasticity in marine invertebrate larvae later in the range from documenting the association between chapter. Phenotypic plasticity is defined as the abil- algal food availability and larval morphology in ity of a genotype to produce different phenotypes different species to examining the ecological and (developmental, physiological, morphological, be- evolutionary implications of the plastic response. havioral, or life history traits) in response to differ- However, investigators have used disparate sys- ent biotic or abiotic environmental factors. Plasticity tems (genera and species of echinoid echinoderms can be adaptive, maladaptive, or effectively neutral. mostly, but also other taxa), employed various When an organism possesses plasticity that confers rearing and measuring techniques and levels of a fitness advantage, then plasticity is considered genetic replication, and relied on different statisti- adaptive. Researchers have focused on examples in cal methodologies for data analysis. They have also which there is evidence that plasticity is adaptive, obtained results ranging from non-plastic to plastic, likely because of the evolutionary and ecological and reached different conclusions about the func- consequences of phenotypes that improve an organ- tional, ecological, and evolutionary roles of pheno- ism’s fitness. However, phenotypic plasticity can be typic plasticity in marine larvae. Our goals with this non-adaptive and still have important ecological chapter are twofold: to review the literature in order consequences (Miner et al., 2005). It is often difficult to help researchers more quickly understand the to experimentally test whether plasticity is adaptive extent and breadth of this field of research, and to because phenotype and environment are typically identify gaps in our understanding in order to pro- confounded, and evidence often comes from both vide guidance for future research. We begin with a experiments and functional arguments. In addition, more general introduction of phenotypic plasticity, adaptation that leads to a fitness advantage (en- and then focus on feeding-structure plasticity in lar- hanced reproductive success of phenotypes across vae of marine invertebrates. generations) is difficult to demonstrate for larval traits of organisms because of the time required to 8.1 Phenotypic Plasticity rear organisms to the adult stage. Plastic pheno- types that are inducible are also classified broadly Research on the expression and evolution of phe- as either defensive or offensive (Miner et al., 2005). notypic plasticity is a rich field, and readers will Plastic phenotypes that protect an organism when find valuable entries into the literature through at risk of death or injury are inducible defenses, the books of West-Eberhard (2003) and DeWitt and whereas those that help an organism gain resources McAlister, J. S. and Miner, B. G., Phenotypic plasticity of feeding structures in marine invertebrate larvae. In. Evolutionary Ecology of Marine Invertebrate Larvae. Edited by Tyler J. Carrier, Adam M. Reitzel, and Andreas Heyland: Oxford University Press (2018). © Oxford University Press. DOI: 10.1093/oso/9780198786962.003.0008 104 EVOLUTIONARY ECOLOGY OF MARINE INVERTEBRATE LARVAE when resources are limiting are inducible offenses. production of the phenotype must be appropriate In some cases, inducible defenses and offenses both to the scale of environmental change (Padilla and occur and are integrated in an organism. Adolf, 1996). There are several general categories of pheno- The degree of plasticity for a given genotype is typic plasticity—developmental, morphological, often measured as either the difference in the mag- physiological, behavioral, or life historical. Re- nitude of phenotypes expressed between two envi- sponses assigned to the same category often have ronments or the slope of the reaction norm across similarities in the timing and reversibility of the environments. The reaction norm for a given geno- response. Morphological changes typically require type depicts graphically the relationship between relatively more time to produce than physiological phenotype and a specific environmental factor. The and behavioral changes. Physiological, behavioral, phenotype is plastic when the slope of the relation- and morphological changes are often, although not ship deviates from zero, and non-plastic (or con- always, reversible when the stimulating environ- stant) when equal to zero. The degree of phenotypic ment is allayed. Changes to an organism’s develop- plasticity can vary among genotypes within a pop- mental trajectory or timing of transitions between ulation. Natural selection can act on this variation, life-history stages can be difficult or impossible to and thus the degree of phenotypic plasticity for a reverse. Though specifically defined responses are given trait is considered a trait in and of itself, with relatively easy to fit into one of these categories, the potential to evolve. Numerous studies have organisms generally respond to their environment documented the expression of phenotypic plastic- with an integrated response of many traits that ity by organisms in general, but fewer have dem- are defined by more than one category. For exam- onstrated variation for plasticity among genotypes ple, some species of plant elongate their stem and both within and among populations, and fewer grow taller when shaded by other plants (West- still have demonstrated that phenotypic plasticity Eberhard, 2003). The response is morphological has evolved in response to environmental changes but is the direct result of underlying physiological and results in higher fitness. Research on pheno- and developmental plasticities. In addition to cause typic plasticity has a long history among terrestrial and effect relationships among plastic responses, plants and insects, and a relatively recent history energy can link different plasticity responses in an among marine invertebrates, particularly in early organism. Responses that require more energy can life stages (e.g., larvae). cause changes in development or life history tran- Marine invertebrates and their larvae face se- sitions, such as metamorphosis from larva to juve- lective pressures in their environments that are nile (West-Eberhard, 2003; Gilbert and Epel, 2015). similar in some ways to those faced by terres- Often, delays in life history transitions result from trial plants and the freshwater juvenile stages of an initial energetically expensive morphological or some terrestrial animals (e.g., predation, compe- physiological plastic response. tition, and dispersal), yet are uniquely different In order for plasticity to evolve, organisms in others (e.g., salinity and CO2-induced ocean must detect reliable cues of environmental change acidification). Also, most freshwater inverte- (chemical, tactile, etc.) and respond at an appro- brate species are taxonomically different, de- priate temporal scale. Thus, plasticity must occur veloping directly and not through larval stages after these cues are received and processed. In or- like marine invertebrates, although a few excep- der for the organism to properly match phenotype tions exist. Thus marine invertebrates and their to environment, these cues must be reliable, pro- larvae constitute a set of research systems that viding information of environmental variability provide a counterpoint to terrestrial and fresh- (e.g., magnitude and frequency). In addition, an water organisms for testing our ideas about the induced phenotype must be well timed with en- biology of phenotypic plasticity. We believe that vironmental change. To ensure that the induced food-induced phenotypic plasticity exhibited by plastic response is effective, the period of time the planktotrophic (i.e., feeding) larvae of many (i.e., lag-time) between sensation of the cue and PHENOTYPIC PLASTICITY OF FEEDING STRUCTURES 105 marine invertebrates provides one of the most and growth, the consequences of plasticity of egg comprehensive examples of phenotypic plasticity organic and energy composition also affect adult among marine organisms. fecundity and lie outside the scope of this review. The duration of larval growth for feeding larvae is influenced by temperature and the availability 8.2 Feeding Larvae of Marine of energetic resources (see Pernet, this volume; Invertebrates Jaeckl e, this volume). In general, higher tempera- tures increase metabolic and growth rates, shorten- The life histories of most species of marine inverte- ing the amount of time individuals spend as larvae brates involve transitions through a series of suc- (O’Connor et al., 2007). Most feeding larvae actively cessive developmental and ontogenetic stages (see acquire and assimilate energy and needed resources Nielsen, this volume). Larvae are typically classi- by capturing and consuming unicellular algae us- fied by whether they can acquire exogenous food ing elaborate ciliated feeding structures, which vary and complete larval development using endog- greatly among taxonomic groups (Strathmann, enous reserves in an egg. Feeding planktotrophic 1987). Exogenous energetic materials
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