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Morphometric Analysis of Surface Utricles in Halimeda Tuna (Bryopsidales, Ulvophyceae) Reveals Variation in Their Size and Symmetry Within Individual Segments

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Morphometric Analysis of Surface Utricles in Halimeda Tuna (Bryopsidales, Ulvophyceae) Reveals Variation in Their Size and Symmetry Within Individual Segments S S symmetry Article Morphometric Analysis of Surface Utricles in Halimeda tuna (Bryopsidales, Ulvophyceae) Reveals Variation in Their Size and Symmetry within Individual Segments Jiri Neustupa * and Yvonne Nemcova Department of Botany, Faculty of Science, Charles University, Prague, 12801 Benatska 2, Czech Republic; [email protected] * Correspondence: [email protected] Received: 26 June 2020; Accepted: 20 July 2020; Published: 1 August 2020 Abstract: Calcifying marine green algae of genus Halimeda have siphonous thalli composed of repeated segments. Their outer surface is formed by laterally appressed peripheral utricles which often form a honeycomb structure, typically with varying degrees of asymmetry in the individual polygons. This study is focused on a morphometric analysis of the size and symmetry of these polygons in Mediterranean H. tuna. Asymmetry of surface utricles is studied using a continuous symmetry measure quantifying the deviation of polygons from perfect symmetry. In addition, the segment shapes are also captured by geometric morphometrics and compared to the utricle parameters. The area of surface utricles is proved to be strongly related to their position on segments, where utricles near the segment bases are considerably smaller than those located near the apical and lateral margins. Interestingly, this gradient is most pronounced in relatively large reniform segments. The polygons are most symmetric in the central parts of segments, with asymmetry uniformly increasing towards the segment margins. Mean utricle asymmetry is found to be unrelated to segment shapes. Systematic differences in utricle size across different positions might be related to morphogenetic patterns of segment development, and may also indicate possible small-scale variations in CaCO3 content within segments. Keywords: continuous symmetry measure; geometric morphometrics; green algae; Halimeda; Ulvophyceae 1. Introduction The green macroalgae of the genus Halimeda J.V.Lamouroux are important calcifying organisms in tropical and sub-tropical marine ecosystems. Their macroscopic thallus is composed of branched filaments (siphons) which contain multiple nuclei but are not divided by any cell walls. Thus, the entire plant represents a single giant multinucleate cell [1]. The above-ground part of the thallus consists of a serial sequence of segments that are separated by short and narrow nodes (see Figure1a). The segments are composed of medullar filaments (located in the central part) and a cortex formed by several layers of swollen utricles. The peripheral (primary) utricles are usually laterally appressed, forming an analogy of an epidermis which separates seawater from the internal interutricular spaces, the prime location of CaCO3 precipitation. Symmetry 2020, 12, 1271; doi:10.3390/sym12081271 www.mdpi.com/journal/symmetry Symmetry 2020, 12, x FOR PEER REVIEW 2 of 15 Symmetryutricles 2020and, 12comparatively, 1271 short lateral adhesion layer, resulting in a shorter diffusion pathway2 of for 15 dissolved ions between the interutricular spaces and the external environment [4]. Figure 1.1. Morphology of Mediterranean H. tuna and surface views of thethe peripheralperipheral utricles:utricles: ( a) a single branch branch of of H.H. tuna tuna consistingconsisting of of four four mature mature segments segments and and one one developing developing protosegment protosegment in the in theapical apical position. position. Note Note that that only only the the mature mature se segmentsgments were were used used in in subsequent morphometricmorphometric analyses. ScaleScale barbar= =5 5 mm; mm; (b )(b segment) segment with with five five positions positions selected selected for the for analyses the analyses of surface of utricles,surface depictedutricles, as:depicted B—bottom, as: B—bottom, C—centre, T—top,C—centre, L—left, T—top, R—right. L—left, Scale R—right. bar = 1 mm;Scale (c )bar microphotograph = 1 mm; (c) showingmicrophotograph surface views showing of peripheral surface views utricles. of peripher Verticesal of autricles. single polygonVertices areof depicted.a single polygon Scale bar are= 75depicted.µm; (d )Scale 6th-order bar = 75 cyclic µm; symmetry (d) 6th-order group cyclic of thesymmetry same polygon group of depicted the same in polygon (c). The depicted vertices of in this (c). size-normalizedThe vertices of this hexagon size-normalized are sequentially hexagon rotated are se aroundquentially the center rotated of around mass of the this center configuration of mass byof 2*pi*ithis configuration/6 radians, where by 2*pi*i/6 i varies radians, from 1 where to 6. Thei varies continuous from 1 to symmetry 6. The continuous measure symmetry (CSM) value measure is the average(CSM) value squared is the distance average between squared the distance original between vertices andthe original the co-ordinates vertices ofand the the perfectly co-ordinates symmetrical of the hexagonperfectly (depictedsymmetrical by blackhexagon stars). (depicted by black stars). TheWhile size interspecific and shape variation of the peripheral in the anatomical utricles vary structure among of species, surface which utricles is one has ofbeen the studied important in identificationdetail for the featurespurpose ofof individual discrimination taxa [among1,2]. Their species size and has beentheir showngenus-level to be taxonomy related to varying[2], the levelsextent ofand CaCO patterns3 tissue of contentinfraspecific among plasticity species in [3, 4these]. It hasfeatures been observedare considerably that taxa less with understood. larger primary The utriclessurface andutricle longer morphology lateral adhesion might layervary tendamong to be di lessfferent calcified individuals, than species among with segments smaller utricles forming and a comparativelydevelopmental short series lateral of a single adhesion plant, layer, or resultingeven among in a shorterthe different diffusion parts pathway of individual for dissolved segments. ions betweenTherefore, the we interutricular specifically focused spaces andon morphometric the external environment analyses of [variation4]. in the shape and size of the surfaceWhile views interspecific of peripheral variation utricles in the in anatomical the Mediterranean structure ofHalimeda surface utriclestuna (J.Ellis has beenand studiedSolander) in detailJ.V.Lamouroux, for the purpose the type of discrimination species of the amongsection species Halimeda and and their the genus-level genus as a taxonomy whole. This [2], thespecies extent is andtypified patterns by tight of infraspecific lateral adhesion plasticity of the in these peripheral features utricles are considerably which form less a understood.honeycomb-like The surface utriclestructure morphology (Figures 1c might and vary2), a amongpattern di sharedfferent individuals,by multiple amongother Halimeda segments taxa. forming This a developmentalpattern results seriesfrom synchronous of a single plant, development or even amongof the peripheral the different utricles parts during of individual segment segments. morphogenesis. Therefore, Surface we specificallyutricles develop focused synchronously on morphometric during analyses segment of variation morphogenesis in the shape by lateral and size expansion, of the surface which views only of peripheralceases when utricles they adhere in the Mediterraneanwith their neighborsHalimeda in the tuna peripheral(J.Ellis and cortex Solander) [1]. J.V.Lamouroux, the type speciesInterestingly, of the section thisHalimeda surface structureand the genusactually as co arresponds whole. This to speciesa Voronoi is typifiedtessellation, by tight which lateral is a adhesionplane partitioned of the peripheral into convex utricles polygons which formsuch athat honeycomb-like each point in surface a given structure polygon (Figures is closer1c and to2 its), agenerating pattern shared point by(seed) multiple than otherto anyHalimeda other [5,6].taxa. The This position pattern of results the seed from in synchronous each utricle developmentis defined by ofits theconstricted peripheral base. utricles In duringthe case segment of ideal morphogenesis. regular positioning Surface of utricles the utricle develop bases synchronously and their Symmetry 2020, 12, 1271 3 of 15 during segment morphogenesis by lateral expansion, which only ceases when they adhere with their neighbors in the peripheral cortex [1]. Symmetry 2020, 12, x FOR PEER REVIEW 4 of 15 Figure 2.2. MicrophotographsMicrophotographs showing showing the the surface surface views views of peripheralof peripheral utricles utricl ofes Mediterranean of MediterraneanH. tuna H. intuna (a) in bottom (a) bottom and (andb) top (b) positions top positions of a single of a single segment. segment. Scale Scale bar = bar50 µ= m.50 µm. 2.2. MorphometricInterestingly, Analysis this surface of Surface structure Utricles actually corresponds to a Voronoi tessellation, which is a plane partitioned into convex polygons such that each point in a given polygon is closer to its generating point In each of the five locations on segments, 30 polygons formed by appressed peripheral utricles (seed) than to any other [5,6]. The position of the seed in each utricle is defined by its constricted base. were randomly selected and their vertices digitized using the TpsDig software, version 2.22 [13]. In the case of ideal regular positioning of the utricle bases and their synchronized developmental timing, Coordinates of the individual polygons are included in Table S1. It should be noted that Halimeda
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