applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Zoological Journal of the Linnean Society, 2019, XX, 1–20. With 6 figures. Choosing the right home: settlement responses by larvae 1.54 of six sea urchin species align with hydrodynamic traits 1.55 1.5 of their contrasting adult habitats JASON HODIN1*, MATTHEW C. FERNER2 and BRIAN GAYLORD3,4 1.60 1Friday Harbor Laboratories, University of Washington, Friday Harbor, WA 98250, USA 1.10 2Estuary & Ocean Science Center, San Francisco State University, Tiburon, CA 94920, USA 3Bodega Marine Laboratory, University of California at Davis, Bodega Bay, CA 94923, USA 4Department of Evolution and Ecology, University of California at Davis, Davis, CA 95616, USA 1.65 Received 13 March 2019; revised 17 September 2019; accepted for publication 24 October 2019 1.15 Ocean organisms as diverse as seaweeds and sea cucumbers exhibit life cycles in which dispersal occurs primarily 1.70 via microscopic larvae or spores, with adults exhibiting limited or even no dispersal. In benthic animals, the larval 1.20 stage concludes with irreversible settlement into the benthos. The decision of where and when to settle is thus one of substantial import. Prior work has shown that settlement in two shoreline echinoids (a sea urchin and a sand dollar) is unexpectedly sensitive to an environmental feature (intense fluid turbulence) that can be considered as a signal to larvae of their arrival in the neighbourhood of the hydrodynamically energetic habitats in which these taxa 1.75 live as adults. Here, we used a comparative approach to explore the evolution of turbulence responsiveness in late- stage echinoid larvae. We examined three pairs of closely related sea urchins that differ in the energetic exposure 1.25 of their adult habitats and found that larval responsiveness to turbulence was more pronounced in urchins that settle in more hydrodynamically exposed locations. These results raise the possibility that evolutionary differences in larval responsiveness to environmental indicators of appropriate adult habitat might reinforce or even provide a mechanism for vicariance in the ocean. 1.80 1.30 ADDITIONAL KEYWORDS: Caribbean geography – deep-sea evolution – distribution – echinoid physiology – Hawaiian Islands – larval behaviour – metamorphosis – rocky shores – sensory perception – sympatric speciation. 1.85 INTRODUCTION In the marine realm there are numerous instances 1.35 of both scenarios for reducing ecological overlap and In the Origin of Species, Darwin noted that closely competition. For example, niche partitioning operates related species tend to be similar in form and habitat, in young-of-the-year rockfish (family Sebastidae) that and thus may compete intensely. This situation often recruit into different subtidal habitats within kelp 1.90 leads to one of two outcomes: one species outcompetes forests (Carr, 1991), whereas allopatry characterizes the other, or one or both species evolve modifications 1.40 related species of snails occupying shallow- vs. deep- to reduce competition (Darwin, 1869). One route to water habitats (e.g. Welch, 2010). the latter outcome is ‘niche partitioning’, which is The biphasic life histories that typify many marine well documented in taxa such as rift-lake cichlids taxa add a layer of complexity to this issue of related 1.95 and Caribbean anole lizards (e.g. Rüber et al., 1999; species avoiding ecological overlap, because adults Losos et al., 2003). Alternatively, competition can be 1.45 and their planktonic larvae often occupy distinct avoided by geographical separation (i.e. allopatry), as habitats. This feature means that although adults of famously exemplified by Darwin’s finches and their congeneric oceanic species may be allopatric—with species-specific use of particular Galápagos Islands different species specializing, for example, in deep sea, 1.100 (Grant, 1999). protected bay or rocky-shore habitats—their larvae 1.50 might nevertheless co-occur during their planktonic *Corresponding author. E-mail: [email protected] period and, in that specific sense, be considered 1.52 1.104 © 2019 The Linnean Society of London, Zoological Journal of the Linnean Society, 2019, XX, 1–20 1 2 J. HODIN ET AL. ‘sympatric’ for a portion of their ontogeny. If those information that could be useful to larvae during larvae then survive and successfully recruit back into settlement (Chia et al., 1981; Ebert, 1982; Fuchs their respective benthic habitats, they re-establish et al., 2004, 2010; Gaylord et al., 2013). For example, allopatry or niche partitioning in each generation high-intensity turbulence produced by large breaking 2.60 2.5 (e.g. Wellenreuther & Clements, 2008), and thus avoid waves occurs most prominently in the surf zones of interspecific competition as adults. rocky shores, is found reliably in few other locations The habitat specificity that maintains geographical and affects settlement of larvae that prefer such separation among biphasic marine taxa would be habitats as adults (Gaylord et al., 2013; Hodin et al., reinforced if larvae are discriminating as to features 2015, 2018b, c; Ferner et al., 2019). The strong vertical 2.65 2.10 of sites they select at the conclusion of their pelagic mixing characteristic of such sites may also interact period. Indeed, there is predicted to be strong with larval responses by enhancing the transport of selection on the processes by which larvae choose larvae to the substratum in these habitats (Denny & a definitive settlement location (Pechenik, 1999); Shibata, 1989), increasing the likelihood that larvae poor decisions by larvae about where and when to will encounter local, seafloor-associated cues. 2.70 2.15 settle would be likely either to be fatal or to result The potential importance of neighbourhood-scale in reduced fitness. It is therefore no surprise that information for larval settlement is reinforced by much work has focused on environmental features recent findings regarding the reactions of larvae to used by larvae to decide where to settle, from the high-intensity turbulence. A mere 30–180 s of exposure presence of olfactory cues indicative of a conspecific can cause echinoid (sea urchin and sand dollar) larvae 2.75 2.20 adult or a required food source, to local flow dynamics to transition immediately from the precompetent suitable for filter feeding, to the texture of a substrate state, in which larvae are not yet responsive to local favourable for burrowing or attachment (Crisp, 1974). settlement cues, to the competent state, in which they Furthermore, it is clear that larvae from different are responsive to such cues and can settle out of the species prioritize different cues, as one would predict plankton (Gaylord et al., 2013; Hodin et al., 2015, 2018c; 2.80 2.25 for larvae searching for habitats tailored to their own Ferner et al., 2019). In this regard, exposure of larvae to needs (Appelbaum et al., 2002; Bierne et al., 2003). intense turbulence, before their arrival at the seafloor, Likewise, larvae respond negatively to cues indicative might prime them to be able to respond quickly and of a poor settlement location (Woodin, 1991), although efficiently to appropriate seafloor-associated chemical negative cues have been less explored. cues once they reach the seabed. 2.85 2.30 Localized settlement cues, both positive and negative, For echinoids, the intensities of turbulence that share the common feature that most are detectable only prompt this shift to competence are comparable to after a larva arrives close to the benthos. For example, those found under breaking waves (George et al., 1994; larvae of species whose adults inhabit wave-exposed Raubenheimer et al., 2004; Gaylord, 2008; Feddersen, shores settle in dynamic intertidal locations where 2012; Gaylord et al., 2013; Sutherland & Melville, 2.90 2.35 breaking waves induce strong water mixing. Beyond 2015). Furthermore, Ferner et al. (2019) recently a few centimetres from such potential settlement reported that this turbulence-induced life-history shift sites, olfactory cues originating at the seabed would be from precompetence to competence is functionally quickly dispersed and diluted (e.g. Denny & Shibata, permanent and is accompanied by a behavioural 1989; Koehl et al., 2007). This situation raises the ‘knockdown’ response, in which larvae remain 2.95 2.40 question as to whether larvae might also exploit temporarily on the substratum after exposure to information available at larger scales, before reaching turbulence (see also Hodin et al., 2018c). Together, the the immediate vicinity of benthic habitat, to increase competence shift and the knockdown response might their chances of arriving and settling there (reviewed increase the likelihood that larvae will both contact by Kingsford et al., 2002; Hodin et al., 2018a). Such an settlement cues on the seafloor and be able to react to 2.100 2.45 ability would not only be selectively advantageous, but them appropriately once they have arrived there. also could contribute to the maintenance of geographical In addition, recently reported genetic variation for separation among species. turbulence responsiveness in the north-east Pacific In fact, a growing body of literature suggests that sand dollar, Dendraster excentricus (Eschscholtz, larvae do respond to cues at broader spatial scales that 1831), suggests that the manner in which echinoid 2.105 2.50 represent the ‘neighbourhood’ of suitable settlement larvae respond to turbulence might be subject to sites. For example, some larvae respond positively selection (Hodin et al., 2018c). When summed, these to characteristic sounds, such as waves impacting findings raise the general hypothesis that larvae from tropical reefs or water flowing over oyster beds related species whose adults occupy distinct habitats (Simpson et al., 2004; Lillis et al., 2013). Wave motions would differ in their responses to neighbourhood-scale 2.110 2.55 and fluid turbulence also provide neighbourhood-scale indicators of those same habitats, in ways that would 2.111 2.56 2.112 © 2019 The Linnean Society of London, Zoological Journal of the Linnean Society, 2019, XX, 1–20 SETTLEMENT CONTRASTS IN SIX URCHIN SPP.