Interspecific Variation in Metamorphic Competence in Marine Invertebrates: the Significance for Comparative Investigations Into the Timing of Metamorphosis Cory D

662 Interspecific variation in metamorphic competence in marine invertebrates: the significance for comparative investigations into the timing of metamorphosis Cory D. Bishop,1,* Megan J. Huggett,* Andreas Heyland,y,§ Jason Hodin,¶ and Bruce P. Brandhorst** *Kewalo Marine Laboratories, 41 Ahui St. Honolulu, HI 96813 USA; yFriday Harbor Laboratories University of Washington, 620 University Road, Friday Harbor, WA 98250 USA; §Whitney Laboratory for Marine Biosciences, University of Florida, 9505 Ocean Shore Blvd, FL 32080 USA; ¶Hopkins Marine Station, Stanford University, Oceanview Boulevard, Pacific Grove, CA, 93950 USA; and **Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, BC V5A 1S6, Canada Synopsis Metamorphosis in marine invertebrate larvae is a dynamic, environmentally dependent process that integrates ontogeny with habitat selection. The capacity of many marine invertebrate larvae to survive and maintain metamorphic competence in the absence of environmental cues has been hypothesized to be an adaptive convergence (Hadfield and others 2001). A survey of the literature reveals that a single generalized hypothesis about metamorphic competence as an adaptive convergence is not sufficient to account for interspecific variation in this character. In an attempt to capture this variation, we discuss the “desperate larva hypothesis” and propose two additional hypotheses called the “variable retention hypothesis” and the “death before dishonor hypothesis.” To validate these additional hypotheses we collected data on taxa from the published literature and performed a contingency analysis to detect correlations between spontaneous metamorphosis, habitat specificity and/or larval life-history mode, three characters relevant to environmentally induced settlement and metamorphosis. In order to account for phylogenetic bias in these correlations, we also constructed a phylogeny of these taxa and again performed a character-correlation analysis. Both these tests suggest that juvenile habitat specificity is correlated to the capacity of individuals to retain the competent larval state in the absence of substrate cues and therefore validate the existence of more than one hypothesis about metamorphic competence. We provide new data from the sea urchin Lytechinus pictus that suggest that nitric oxide (NO) and thyroxine hormone signaling interact to determine the probability of settlement in response to a settlement cue. Similarly, we provide evidence that thyroxine signaling in the sand dollar Dendraster excentricus increases spontaneous metamorphosis in the absence of cues from adult conspecifics in a manner that is independent of larval age. Introduction In marine invertebrates, hatching results either in a which an environmentally mediated irreversible small version of the adult or an intermediate stage, commitment to transform from the larval to the usually called a larva. In the latter case, both larval juvenile stage has occurred. and presumptive juvenile tissues continue to grow and In order for habitat selection to coincide with develop to varying degrees until a stage referred to as metamorphosis, the competent larval state must be “competence” is reached. Competence is operationally retained until suitable substrates are found. The defined as the capacity of a developing individual to competent stage, and the corresponding retention of initiate settlement and complete morphogenetic the larval state in the absence of cues, therefore transformations associated with metamorphosis. In represents an example of developmental plasticity. many cases this requires reception of environmental Accordingly, the term “delay of metamorphosis” cues (for example, substrate-derived physical or is used extensively (Pechenik 1990 for review) to reflect chemical cues that indicate habitat quality). We use this plasticity in the developmental process. Here we the term metamorphosis to refer to the point at use “retention of the larval state” synonymously with From the symposium “Metamorphosis: A Multikingdom Approach” presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2006, at Orlando, Florida. 1 E-mail: [email protected] Integrative and Comparative Biology, volume 46, number 6, pp. 662–682 doi:10.1093/icb/icl043 Advance Access publication September 28, 2006 Ó The Author 2006. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. Metamorphic competence in marine invertebrates 663 “delay of metamorphosis” or any other such terms instead of simply leading to death. When should describing this phenomenon. In our use of the word energetic limitations lead to a decrease in selectivity “retention” we are not referring to the physical or spontaneous metamorphosis? retention of larvae close to the hatching site. If one assumes that desperate larval behavior in A principal point of interest in this work is the general is adaptive, it should be selected to arise during existence of broad patterns in the response of the competent period at the point when the benefits of competent larvae to the absence of cues, as a function retaining the larval state are offset by any combination of time. Upon close examination of the many of (1) larval mortality, (2) insufficient reserves to examples in the literature of developmental plasticity complete metamorphosis even if suitable habitats are that fall under the rubric of delay of metamorphosis, encountered, (3) decreases in post-metamorphic one finds that the dynamics of this phenomenon show performance, or (4) diminishing returns for continued considerable diversity. In particular, there is variation dispersal. Additional support for the desperate larva among taxa in the degree to which larvae can retain hypothesis will come from (1) a correlation of larval the competent larval state in the absence of cues and size and energetic content; (2) an understanding of the food, and correspondingly, the degree to which the mechanism by which a decrease in energetic content specificity of cues required for metamorphosis is transduced into a morphogenetic output; (3) inte- changes over time. The evolutionary and ecological gration with data such as those from Eri and ramifications of these differences in the retention of others (1999), who demonstrated that in the ascidian the competent larval state have been the subject of Herdmania curvata, competence is correlated with the much theoretical consideration and speculation (for anterior expression of Hemps, an EGF-like protein; example, Pechenik 1990, 2006; Pechenik and others and (4) evidence that ecologically meaningful delays 1998). Based upon our own ideas, as well as those in result in changes in larval selectivity. the literature, we have organized these differences into three hypotheses. We explore the idea that, as a character, competence varies in the degree to which it The “variable retention” hypothesis is continuous, and that this variation is ultimately It is clear from several laboratory studies (see Table 2) interpretable both in the context of ecological factors that feeding larvae can also display a tendency toward (such as juvenile habitats and larval feeding mode) spontaneous settlement and metamorphosis as a and of underlying signaling systems that control the function of time in the competent state. This may timing of the metamorphic “decision.” involve the gradual increase in an internal stimulatory factor, or the gradual decrease of an inhibitory factor, or both. Again, this general idea is not new, but details of “Desperate larva” hypothesis the identity and function of such stimulatory and Tested recently by Marshall and Keough (2003) and inhibitory factors that can account for observed Toonen and Pawlik (2001), but suggested originally by behaviors have thus far been slow to accumulate (but the data of Wilson (1953) and Knight-Jones (1953), see Berking 1988; Welborn and Manahan 1995; and data the desperate larva hypothesis refers to the idea that, below). In contrast to the “desperate larva” hypothesis, as energetic reserves decline during the competent the “variable retention” tendency is less likely to be period, metamorphosis occurs in response to a non- linked to food limitation. Nevertheless, it is possible for specific cue or even in the absence of any known feeding larvae to become energy-limited either because substrate cue (for example, clean plastic or glass or the of increases in metabolic demands from developing air/water interface). Marshall and Keough (2003) juvenile tissues or because of patchy food resources. indirectly verified this idea by showing that larvae Fenaux and Pedrotti (1988) provided documenta- from two bryozoan and one ascidian species having tion of planktonic metamorphosis in four species of lecithotrophic development settled spontaneously in a echinoids, indicating a low capability of these species size-specific manner: larger larvae had longer swim- to retain the larval state in the absence of cues from ming periods, indicating greater capacity (presumably juvenile habitats. When data from all species and because of greater maternal provisioning) for retain- sampling points were pooled, post-larvae (that is, ing the larval state. Inherent in this hypothesis is the juveniles) represented an average of 9% of the total idea that the mechanism that initiates metamorphosis sample collected from the

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