Environmental influences on the Indo-Pacific octocoral Isis hippuris Linnaeus 1758 (Alcyonacea: Isididae): genetic fixation or phenotypic plasticity?

Abstract

As conspicuous modular components of benthic marine habitats, gorgonian (sea fan) octocorals have perplexed taxonomists for centuries through their shear diversity, particularly throughout the Indo-Pacific. Phenotypic incongruence within and between seemingly unitary lineages across contrasting environments can provide the raw material to investigate processes of disruptive selection. Two distinct phenotypes of the Isidid Isis hippurisLinnaeus, 1758 partition between differing reef environments: long-branched bushy colonies on degraded reefs, and short-branched multi/planar colonies on healthy reefs within the Wakatobi Marine National Park (WMNP), Indonesia. Multivariate analyses reveal phenotypic traits between morphotypes were likely integrated primarily at the colony level with increased polyp density and consistently smaller sclerite dimensions at the degraded site. Sediment load and turbidity, hence light availability, primarily influenced phenotypic differences between the two sites. This distinct morphological dissimilarity between the two sites is a reliable indicator of reef health; selection primarily acting on colony morphology, porosity through branching structure, as well as sclerite diversity and size. ITS2 sequence and predicted RNA secondary structure further revealed intraspecific variation between I. hippuris morphotypes relative to such environments (ΦST = 0.7683, P < 0.001). This evidence suggests-but does not confirm-that I. hippuris morphotypes within the WMNP are two separate species; however, to what extent and taxonomic assignment requires further investigation across its full geographic distribution. Incongruence between colonies present in the WMNP with tenuously described Isis alternatives (Isis reticulataNutting, 1910, Isis minorbrachyblastaZou, Huang & Wang, 1991), questions the validity of such assignments. Furthermore, phylogenetic analyses confirm early taxonomic suggestion that the characteristic jointed axis of the Isididae is in fact a convergent trait. Thus the polyphyletic nature of the Isididae lies in its type species I. hippuris, being unrelated to the rest of its family members.

Keywords: Gorgonian coral; ITS2; Indonesia; Isididae; Isis hippuris; Morphology; Wakatobi Marine National Park (WMNP).

Figure 1. Isis hippuris morphotypes and location map of the Wakatobi Marine National Park (WMNP), SE Sulawesi, Indonesia.

Isis hippuris morphotypes: (A) short branched predominantly planar or multiplanar colonies at the healthy site Ridge 1, and (B) long branched bushy colonies at the impacted site Sampela, with additional (C) collection localities within the WMNP. Sample number in brackets for molecular and asterisk for morphological analyses.

Figure 2. Isis hippuris morphological trait measurements plate.

Isis hippuris morphological trait measurements of the (A) colony; (B, C, D) canal and polyp dynamics; (E) sub-colony (branching) dynamics; (F) sclerites site/morphotype comparisons of i and ii spindles, iii and iv capstan 7-radiates, v–vi and vii–viii clubs from Ridge 1 and Sampela respectively. All abbreviations are described in text.

Figure 3. Constrained ordinations (CAP) of Isis hippuris character traits.

Constrained ordinations (CAP) of Isis hippuris character traits between Ridge 1 [◆] and Sampela [▴]. Vector abbreviations as described in text.

Figure 4. Isis haplotype network and ITS2 RNA predicted secondary structure.

Isis haplotype network with corresponding ITS2 RNA predicted secondary structure relative to haplotype ((A–E), see also Fig. 5) and enthalpy values according to MFOLD. Roman numerals (I–IV) represent helices; red and black arrows indicate point mutations and loop differences, respectively. Coloured bases according to transitions (red), transversions (yellow) and gaps (lilac), S5. Haplotype circle diameters are proportional to identical clone sequences.

Figure 5. Phylogram of Isis haplotypes and Octocoral out groups.

Phylogram based on Maximum Likelihood (ML) analyses of the ITS2 region from twenty Octocoral taxa in GenBank and Isis haplotypes within the WMNP. Branch numbers represent ML bootstrap support and BI posterior probabilities, respectively, with low values expressed as a hyphen (–) ≤70% and asterisk (*) indicative of differences from MrBayes phylogenetic inference. Letters Sc, Scleraxonia; Ca, Calcaxonia, Ho, Holaxonia, Al, Alcyoniina, and A–E represent Isis haplotypes as depicted in Fig. 4.