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Adaptive Specialization and Constraint in Morphological Defences of Planktonic Larvae

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Adaptive Specialization and Constraint in Morphological Defences of Planktonic Larvae Received: 30 April 2019 | Accepted: 1 October 2019 DOI: 10.1111/1365-2435.13464 RESEARCH ARTICLE Adaptive specialization and constraint in morphological defences of planktonic larvae Samuel M. Bashevkin1 | John H. Christy2 | Steven G. Morgan1 1Bodega Marine Laboratory and Department of Environmental Science Abstract and Policy, University of California, Davis, 1. Morphological defences of plankton can include armour, spines and coloration. Bodega Bay, CA, USA Spines defend from gape-limited fish predators, while pigmentation increases vis- 2Smithsonian Tropical Research Institute, Panamá, República de Panamá ibility to fishes but defends from ultraviolet radiation (UVR). 2. Planktonic crab larvae (zoeae) exhibit inter- and intraspecific variability in the Correspondence Samuel M. Bashevkin lengths of defensive spines, extent of pigmentation and body size. The deter- Email: [email protected] minants of this variability and the relationships among these traits are largely Present address unknown. Samuel M. Bashevkin, Delta Science 3. Larvae may employ generalized defences against the dual threats of UVR and pre- Program, Delta Stewardship Council, Sacramento, CA, USA dation or specialized defences against their primary threat, with an unknown role of allometric or phylogenetic constraints. Generalization would result in longer Funding information National Geographic Young Explorer's spines compensating for the increased predation risk imposed by darker pigments, Grant; American Museum of Natural History while specialization would lead to more investment in either defence from preda- Lerner-Gray Fund for Marine Research; UC Davis Hemispheric Institute of the Americas tion (long spines) or UVR (dark pigments), at the expense of the other trait. Tinker Summer Field Research Grant; UC 4. We examined (a) the relationship between spine lengths and pigmentation, (b) the Davis Jastro Shields Graduate Research Fellowship; Smithsonian Tropical Research scaling of spine lengths with body size, and (c) phylogenetic constraint in spine Institute Short Term Fellowship; National lengths, pigmentation, and body size, among and within 21 species of laboratory- Defense Science and Engineering Graduate Fellowship hatched and 23 species of field-collected crab larvae from Panama and California. 5. We found a negative relationship between spine length and pigmentation among Handling Editor: Susana Clusella Trullas species from laboratory and field. Within species, we found a marginally signifi- cant negative relationship among field-collected larvae. 6. Spine lengths showed positive allometric scaling with carapace length, while spine and carapace lengths, but not pigmentation, had significant phylogenetic signals. 7. The negative relationship we observed between pigmentation and spine length supports our defence specialization hypothesis. 8. Positive allometric scaling of spine lengths means larger larvae are better de- fended from predators, which may indicate that larvae face greater predation risk as they grow larger. 9. Phylogenetic constraint may have arisen because related species encounter simi- lar predation threats. Conversely, phylogenetic constraint in the evolution of spine lengths may induce convergent behaviours resulting in related species facing simi- lar predation threats. Functional Ecology. 2019;00:1–12. wileyonlinelibrary.com/journal/fec © 2019 The Authors. Functional Ecology | 1 © 2019 British Ecological Society 2 | Functional Ecology BASHEVKIN ET AL. 10. Our results improve understanding of the evolution of the larval morphology of crabs, morphological defences in the plankton and evolutionary responses of morphology to multiple spatially segregated selective forces. KEYWORDS allometry, coloration, comparative phylogenetics, crab, marine, predation, ultraviolet radiation, zoea 1 | INTRODUCTION Like Daphnia, larval crabs have defensive spines that deter gape- limited predators such as fishes (Morgan, 1987, 1989, 1990). Larval Morphological defences can take a number of forms. Common ex- crabs are also pigmented to reduce UVR damage but these pig- amples include the hard armour plating of armadillos (Superina & ments may increase susceptibility to visual predators, such as fishes Loughry, 2012), crustacean carapaces (Fryer, 1968), sharp porcupine (Bashevkin et al., 2019b; Morgan & Christy, 1996; Bashevkin, Christy, quills (Quick, 1953) and Daphnia (water flea) spines (Dodson, 1984). & Morgan, in review). Both pigmentation and spine length show con- In addition, pigmentation may camouflage from predators (Merilaita, siderable variation among species of crabs, as well as some variation Scott-Samuel, & Cuthill, 2017) or defend from ultraviolet radiation within species. Some variability in spine length may be related to the (Bandaranayake, 2006). These features are common in terrestrial, level of predation risk in larval habitats (Morgan, 1990), but we do aquatic and marine habitats, although the optimal defence may vary not yet know whether spine lengths are related to pigmentation, how with habitat type. For example, while terrestrial camouflage often spine lengths scale with body size or how constrained these traits may involves some form of pigmentation to match backgrounds or con- be by phylogeny (i.e. are these traits free to evolve or are they con- fuse predators, the best camouflage in aquatic and marine habitats strained by their evolutionary history to be similar to related species?). is often transparency or the lack of pigmentation (Johnsen, 2001; Better knowledge of the drivers of morphological variability in McFall-Ngai, 1990; Stevens & Merilaita, 2009). larval crabs will improve our understanding of crab larval distribu- Morphological defences often have costs. Armadillos carrying a tions, survival, and dispersal and, more generally, the evolution of heavy carapace move (and thus feed) slowly and must spend most of morphological defences. Understanding the adaptive benefits of their active time feeding (Superina & Loughry, 2012). Spines grown morphological features can help identify sources of selection on by Daphnia in the presence of predators slow growth in the rest of larvae of understudied species based on their morphology. Since the body and delay reproductive maturity (Riessen & Sprules, 1990). UVR and visual predation are both vertically stratified threats con- Transparent camouflage in marine and aquatic plankton increases centrated in the upper surface of the water column, a better un- mortality from ultraviolet radiation (Bashevkin, Christy, & Morgan, derstanding of the traits affecting vulnerability to these sources of 2019b; Hairston, 1976; Morgan & Christy, 1996). mortality could improve understanding of larval vertical distribu- Morphological defences vary considerably both within and among tions that determine horizontal dispersal (Morgan, 2014; Queiroga species. Some of this variation may be related to the environment. & Blanton, 2005). Defining the scaling relationship of spine lengths Daphnia grow long spines in the presence of predator cues (Krueger with body size will help us understand how changing ocean condi- & Dodson, 1981) and copepods maintain transparency in lakes with tions altering body sizes (Bashevkin et al., in press) may also impact low UVR and high fish predation risk but increase pigmentation predator defence. A phylogenetically controlled analysis of these when conditions are reversed (Hairston, 1976; Hansson, Hylander, & morphological defences will improve our understanding of their evo- Sommaruga, 2007; Hylander, Souza, Balseiro, Modenutti, & Hansson, lution and constraints on adaptation to shifting threats. 2012). Morphological variation can also be driven by differences in Ultraviolet radiation at relevant field intensities has substantial genetics, maternal investment or other factors resulting in a range lethal and sublethal effects on marine organisms, including larval of morphologies in a common environment (Monteiro et al., 2000). crabs (Bancroft, Baker, & Blaustein, 2007; Bashevkin et al., 2019b). Variation in offspring size within broods, among broods and among While visual predation and UVR are both concentrated in surface species would influence the size and thereby efficacy of morpholog- waters, visual fish predation is more intense in shallow nearshore ical defences such as spines. The effect of this size variation would habitats with high productivity (Morgan, 1986, 1990) and UVR is strongly depend on the nature of the scaling of the defensive fea- more intense in clear offshore waters with low productivity (Tedetti ture with body size. Positive allometry would confer disproportion- & Sempéré, 2006). This vertical overlap but horizontal segregation ately greater predator defence with larger body size while negative of threats suggests that crab larvae may employ either defence gen- allometry, as is found in Daphnia (Lampert & Wolf, 1986; Smakulska eralization or specialization. If larvae are generalizing and adopting & Górniak, 2004), would confer disproportionately greater predator the best defence from both threats, pigmented larvae would mor- defence to smaller body sizes. Furthermore, the optimal spine length phologically compensate for increased predation risk by growing would depend on the size distribution of gape-limited predators. longer spines, resulting in a positive relationship between these BASHEVKIN ET AL. Functional Ecolo gy | 3 traits. Conversely, if larvae are specializing, larvae would invest more centrifugal pump at 30 m3/h into a
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