Larouche-Bilodeau C et al. (2020), Filter feeding, deviations from bilateral symme...

ECB-ART-49432

Ecol Evol 2020 Nov 03;1023:13544-13554. doi: 10.1002/ece3.6962.

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Filter feeding, deviations from bilateral symmetry, developmental noise, and heterochrony of hemichordate and cephalochordate gills.

Larouche-Bilodeau C , Guilbeault-Mayers X , Cameron CB .

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We measured gill slit fluctuating asymmetry (FA), a measure of developmental noise, in adults of three invertebrate deuterostomes with different feeding modes: the cephalochordate Branchiostoma floridae (an obligate filter feeder), the enteropneusts Protoglossus graveolens (a facultative filter feeder/deposit feeder) and Saccoglossus bromophenolosus (a deposit feeder). FA was substantially and significantly low in B. floridae and P. graveolens and high in S. bromophenolosus. Our results suggest that the gills of species that have experienced a relaxation of the filter feeding trait exhibit elevated FA. We found that the timing of development of the secondary collagenous gill bars, compared to the primary gill bars, was highly variable in P. graveolens but not the other two species, demonstrating an independence of gill FA from gill bar heterochrony. We also discovered the occasional ectopic expression of a second set of paired gills posterior to the first set of gills in the enteropneusts and that these were more common in S. bromophenolosus. Moreover, our finding that gill slits in enteropneusts exhibit bilateral symmetry suggests that the left-sidedness of larval cephalochordate gills, and the directional asymmetry of Cambrian stylophoran echinoderm fossil gills, evolved independently from a bilaterally symmetrical ancestor.

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	Figure 1. Photographs of (a) Saccoglossus bromophenolosus, (b) Protoglossus graveolens, and (c) Branchiostoma floridae. (a) and (b) were live specimens. (c) was stained and cleared. Scale bars equal 4 mm
	Figure 2. Line drawing of the developmental stages of the gill slits and bars. Note that gill pores are ectodermal and drawn as solid lines, whereas gill slits and bars are endodermal and the slits are drawn as dotted lines. (a) Early gill slits are round in circumference and bordered by small lateral primary gill bars. (b) The primary gill bars develop around the gill slit elongating it to form the early stage secondary gill bars. (c) The secondary gill bars elongate ventrally, dividing the primary gill slit into two elongated secondary gill slits. (d) The secondary gill bars are fully developed. Gill slits are numbered in each drawing representing how we counted them gp, gill pore; pb, primary gill bar; ps, primary gill slit; sb, secondary gill bar; ss, secondary gill slit
	Figure 3. Graphical representation of the distribution of the symmetry index (R‐L) for each species. Saccoglossus bromophenolosus (Hemichordata) is a deposit feeder, Protoglossus graveolens (Hemichordata) is a facultative filter feeder, and Branchiostoma floridae (Cephalochordata) is an obligate filter feeder. S. bromophenolosus, P. graveolens, and B. floridae have symmetry index distribution means of 0.15, 0.08, and −0.26 and symmetry index distribution standard deviations of 2.57, 1.12, and 0.80, respectively
	Figure 4. Differences (a) in number of gill slits and (b) symmetry index (R‐L) squared residuals among species. Error bars represent the 95% confidence intervals; letters above each mean represent Tukey’s honest significant difference (HSD) groupings (p ≤ .05)
	Figure 5. Representation of the two modes of the distribution of the symmetry index (R‐L) for each species (a) in the skewness, and (b) the kurtosis. S. bromophenolosus, P. graveolens, and B. floridae have a kurtosis of 7.25, 5.78, and 5.59, and a skewness of 0.23, 0.19, and −0.69, respectively. The distribution of the skewness and the kurtosis was calculated from 10,000 rounded normal distribution (µ = −0.01, σ = 1.50). In panel (a), the vertical lines beginning from the left represent the 5% quantile and the 95% quantile, respectively, and in panel (b), the vertical line represents the 95% quantile. The deposit feeder is S. bromophenolosus, the facultative filter feeder is P. graveolens, and the obligate filter feeder is the cephalochordate B. floridae
	Figure 6. Photographs of the gill slit complexes of (a) Saccoglossus bromophenolosus, (b) Protoglossus graveolens, and (c) Branchiostoma floridae. (d) S. bromophenolosus gill slits complex in higher magnification, and (e) underdeveloped secondary gill slits following damage, and (f) a second ectopic gill complex posterior to the normal complex. Anterior is at the top with a section of cleared intestine in between. All scale bars equal 500 µm except for (b) were the scale bars equal 1,000 µm. In all photograph, the pharynx midline is dorsal except (c) where it is ventral. eg, ectopic gills; pb, primary gill bar; ps, primary gill slit; s, synapticula; sb, secondary gill bar; ss, secondary gill slit; ug, underdeveloped gill bar

References [+] :

Boorman, The evolution of left-right asymmetry in chordates. 2002, Pubmed