Hodin J et al. (2016), A newly identified left-right asymmetry in larv...

ECB-ART-45022

R Soc Open Sci 2016 Aug 31;38:160139. doi: 10.1098/rsos.160139.

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A newly identified left-right asymmetry in larval sea urchins.

Hodin J , Lutek K , Heyland A .

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Directional asymmetry (DA) in body form is a widespread phenomenon in animals and plants alike, and a functional understanding of such asymmetries can offer insights into the ways in which ecology and development interface to drive evolution. Echinoids (sea urchins, sand dollars and their kin) with planktotrophic development have a bilaterally symmetrical feeding pluteus larva that undergoes a dramatic metamorphosis into a pentameral juvenile that enters the benthos at settlement. The earliest stage of this transformation involves a DA: a left-side invagination in mid-stage larvae leads to the formation of the oral field of the juvenile via a directionally asymmetric structure called the echinus rudiment. Here, we show for the first time in two echinoid species that there is a corresponding DA in the overall shape of the larva: late-stage plutei have consistently shorter arms specifically on the rudiment (left) side. We then demonstrate a mechanistic connection between the rudiment and arm length asymmetries by examining rare, anomalous purple urchin larvae that have rudiments on both the left and the right side. Our data suggest that this asymmetry is probably a broadly shared feature characterizing ontogeny in the class Echinoidea. We propose several functional hypotheses-including developmental constraints and water column stability-to account for this newly identified asymmetry.

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Genes referenced: kin LOC100887844 LOC100893907

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	Figure 1. Larvae of the sand dollar D. excentricus show directional asymmetry in postoral arms. (a) Representative D. excentricus larva at 9 days postfertilization, with four pairs of larval arms. Note that the left side of the larva is the side of the well-developed juvenile rudiment (dark region labelled ‘Rud’ in this image); as this is a ventral view, the ‘left’ side of the larvae is seen here on the right side of the image, and vice-versa; scale bar: 100 µm. (b) Schematic of a sand dollar pluteus larva with four pairs of larval arms, with the coloured lines indicating the measurements taken for this study, oriented as in (a). (c) Mean larval arm length in µm for all four larval arms at day 9; n = 20 larvae. Lighter bars: right arms; darker bars: left arms. (d) Mean index of asymmetry [ln(R/L)] for all arm pairs; positive values indicate right-based asymmetry (i.e. longer arms on the right side); negative values indicate left-biased asymmetry. PO: postoral arms; PD: posterodorsal arms; ALA: anterolateral arms; PRO: preoral arms. Asterisks in (d) indicate significant differences (p < 0.05) between left and right side, and therefore directional asymmetry (DA). Error bars are one standard error of the mean.
	Figure 2. Directional asymmetry in purple urchin (Str. purpuratus) larvae as a function of age. We analysed left–right asymmetry in larval arms as a function of age during late-larval development for the (a) postoral, (b) anterolateral, (c) posterodorsal and (d) preoral arm pairs (on day 15, these larvae had only six arms; hence the absence of data for PRO arms on that day). Graphs in (a–d) have two y-axes: the primary (left) axis shows larval arm length in micrometres for all four larval arms, as is seen in the data points connected by dark solid (left arm) and dashed grey (right arm) lines. The secondary (right) axis shows the mean index of asymmetry [ln(R/L)], as is seen in the grey bars. (e) Schematic as in figure 1b repeated for convenience. The cross-polarized light micrograph in (f') shows a representative early stage larva (day 15, stage bin A; see figure 3), and in (f''), a representative late-stage larva (day 39, stage bin F; see figure 3). Note the visible juvenile skeleton (on the left side; pictured in the right side of these ventral views) and clear L–R arm asymmetry in (f'') but not (f'). Time is in days postfertilization (PF), Scale bars in (e,f), 150 µm. Abbreviations, asterisks and error bars as in figure 1. See table 1 for statistics.
	Figure 3. Directional asymmetry in purple urchin larvae as a function of juvenile rudiment stage. We analysed left–right asymmetry in larval arms as a function of juvenile rudiment stage for the (a) postoral, (b) anterolateral, (c) posterodorsal and (d) preoral arm pairs. We binned juvenile rudiment stages after [22] as follows: bin A, skeletogenic stage 0; bin B, skeletogenic stages 1–2; bin C, skeletogenic stages 3–4; bin D, skeletogenic stages 5–6; bin E, skeletogenic stages 7–8; bin F, skeletogenic stages 9–10. Double axes and line colours as in figure 2. Abbreviations, asterisks and error bars as in figure 1. See table 2 for statistics.
	Figure 4. Directional asymmetry in total arm length of purple urchin larvae as a function of age and juvenile rudiment stage. We summed the length of the four pairs of arms on the right and left sides, and compared them by age (a) and juvenile rudiment stage (b). Note the lack of a monotonic increase in asymmetry as development proceeds, especially in (b). Double axes and line colours as in figure 2. Abbreviations, asterisks and error bars as in figure 1. Stage bins as in figure 3. See tables 1 and 2 for statistics.
	Figure 5. Reduced larval food does not alter directional asymmetries in arm length across stages. (a–d) We detected asymmetry in arm lengths with stage under both high food (HF; upper graphs in each panel) and low food (LF; lower graphs) conditions in purple urchins, with no detectable differences in any arm pair between high and low food (see the text). Double axes and line colours as in figure 2. Abbreviations, asterisks and error bars as in figure 1. Stage bins as in figure 3. Numbers of larvae at each stage are as follows. Stage bin A: HF, n = 0; LF, n = 4. Stage bin B: HF, n = 3; LF, n = 18. Stage bin C: HF, n = 6; LF, n = 9. Stage bin D: HF, n = 13; LF, n = 17. Stage bin E: HF, n = 8; LF, n = 18. Stage bin F: HF, n = 15; LF, n = 8. Note that there were no HF larvae in stage bin A, presumably due to their more rapid development than in the corresponding low food larval cohort.
	Figure 6. Larval arms of anomalous purple urchin larvae with double rudiments are more symmetrical. We analysed the index of arm-length asymmetry (see figure 1 legend) in naturally occurring larvae with juvenile rudiments on both the left and right sides (double rudiments; (b), as compared to their full siblings with single rudiments (c). Cartoons along bottom of figure indicate single and double rudiments. (a) Whereas larvae with single rudiments (n = 9 larvae) in this experiment showed right-biased directional asymmetry (positive values) in postoral (PO) and posterodorsal (PD) arms (asterisks in right half of (a)), stage-matched larvae with double rudiments (n = 8 larvae) did not show right-biased asymmetry in any of their arm pairs; in fact PO arms in double-rudiment larvae showed left-biased asymmetry (negative values; asterisk in left half of (a)). Scale bars in (b,c): 150 µm. Abbreviations, asterisks, error bars and orientation of larvae as in figure 1.

References [+] :

Adomako-Ankomah, P58-A and P58-B: novel proteins that mediate skeletogenesis in the sea urchin embryo. 2011, Pubmed, Echinobase