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R Soc Open Sci
2015 Jun 01;26:150114. doi: 10.1098/rsos.150114.
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Rethinking competence in marine life cycles: ontogenetic changes in the settlement response of sand dollar larvae exposed to turbulence.
Hodin J
,
Ferner MC
,
Ng G
,
Lowe CJ
,
Gaylord B
.
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Complex life cycles have evolved independently numerous times in marine animals as well as in disparate algae. Such life histories typically involve a dispersive immature stage followed by settlement and metamorphosis to an adult stage on the sea floor. One commonality among animals exhibiting transitions of this type is that their larvae pass through a ''precompetent'' period in which they do not respond to localized settlement cues, before entering a ''competent'' period, during which cues can induce settlement. Despite the widespread existence of these two phases, relatively little is known about how larvae transition between them. Moreover, recent studies have blurred the distinction between the phases by demonstrating that fluid turbulence can spark precocious activation of competence. Here, we further investigate this phenomenon by exploring how larval interactions with turbulence change across ontogeny, focusing on offspring of the sand dollar Dendraster excentricus (Eschscholtz). Our data indicate that larvae exhibit increased responsiveness to turbulence as they get older. We also demonstrate a likely cost to precocious competence: the resulting juveniles are smaller. Based upon these findings, we outline a new, testable conception of competence that has the potential to reshape our understanding of larval dispersal and connectivity among marine populations.
Figure 1. Schematic of null and alternative hypotheses for ontogenetic changes in the turbulence response. We here envision a series of hypotheses to account for changes in how larvae respond to turbulence as ontogeny proceeds. Each of the panels shows how the proportion of sand dollar larvae that settle following exposure to turbulence might change as a function of turbulence intensity, for three different larval ages (day 9 through day 11 after fertilization). From each of the dose–response curves shown, we can calculate the maximal proportion of larvae induced on that day (lower case Greek letters), as well as the turbulence intensity at which larvae become sensitive to turbulence exposure, represented by the inflection point of the curve (upper case Greek letters). See text for a full explanation of each hypothesis.
Figure 2. Representative precompetent and competent D. excentricus larvae. (a) Advanced precompetent larva, 11 days after fertilization (20–22°C). The rudiment is the dark area on the left side of the central body region; the stomach is the reddish area on the right side. (b) Early competent larva, 12 days after fertilization, at the same magnification as in (a). Note the shrunken larval arms, more rotund morphology, and the rudiment filling the entire central body region, all typical of competent larvae of these sand dollars. Inset shows a cross-polarized light magnified view of three developing adult-type spines within the rudiment of this larva. (c) Juvenile, at the same magnification as in (a) and (b), settled in response to 40 mM excess KCl (without turbulence exposure) on day 14, photographed on day 15. Scale bars: (a–c) 100 μm; (b) inset, 25 μm.
Figure 4. Sand dollar larvae show substantial batch-to-batch variation in the turbulence response across ontogeny. (a) Larval batch A, fertilized 27 May 2014. (b) Larval batch B, fertilized 28 May 2014. Each of the data points in (a) and (b) are results from single runs of 25 larvae, with the exception of the day 9 batch A data, which we replicated once (data points on day 9 in (a) show the mean of the two runs; error bars are s.e.m). (c) Larval batch C, fertilized 22 August 2014. Each of these data points are means of four runs at each speed with 20–25 larvae each; error bars are s.e.m. Note that in (a–c), we do not indicate the error along the x-axis in each of the Taylor–Couette cell rotation rates that we employed, which we estimate to be approximately ±25 r.p.m. Each graph shows the energy dissipation rates (in W kg−1) on the lower x-axis, and the corresponding rotation rates (spin speeds in r.p.m.) along the upper x-axis. We only tested day 7 larvae from batch A and day 10 larvae from batches A and B.
Figure 6. Precompetent sand dollar larvae show evidence of increasing sensitivity to turbulence as ontogeny proceeds. (a) Shown are the best-fit curves (solid curves) ±95% CIs (dashed curves) generated by our best-supported general mixed linear model (see Material and methods for details and comparisons with other models). The lines and symbols (batch A, squares; batch B, circles; batch C, crosses) show the data from day 9 (black) and day 11 (grey). Error bars are s.e.m (note that the data from batch A day 11 and batch B days 9 and 11 were unreplicated, thus show no error bars). The inflection points of the best-fit curves for day 9 (black arrow) and day 11 (grey arrow) are shown along the x-axis and indicated by the black and grey vertical dotted lines, respectively. The shaded areas within the day 9 and day 11 CI curves indicate the range of 95% CIs in our respective inflection point estimates based upon 10 000 non-parametric bootstrap samples. (b) The range of inflection point estimates (and 8.5% overlap) from these bootstrap samples on days 9 and 11. Arrows as in (a). Note that the y-axis units of density are linearly related to the proportion of bootstrap samples showing a given range of inflection point estimates.
Figure 8. Precompetent larvae primed by turbulence exposure settle at a smaller size. (a) Mean test area in 12-day-old juveniles (n=49) deriving from turbulence exposure (approx. 2 W kg−1 for 3 min) while precompetent, compared to 15-day-old competent juveniles (n=29) never exposed to turbulence. Shown are standard Tukey box plots with the dots as outliers. Representative 12-day-old turbulence-exposed juvenile (b) and 15-day-old control juvenile (c) from this experiment, photographed at the same magnification. White dotted lines indicate the major and minor axes of the ellipses used to estimate cross-sectional test area. Note also the relatively shorter spines in (b), another indication of the precocious state of these turbulence-induced juveniles. Scale bars, 100 μm. The effect size here (mean size on day 15 − mean size on day 12) is 19 437 μm2.
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