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A Case of Modular Phenotypic Plasticity in the Depth

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A Case of Modular Phenotypic Plasticity in the Depth View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Springer - Publisher Connector Calixto-Botía and Sánchez BMC Evolutionary Biology (2017) 17:55 DOI 10.1186/s12862-017-0900-8 RESEARCH ARTICLE Open Access A case of modular phenotypic plasticity in the depth gradient for the gorgonian coral Antillogorgia bipinnata (Cnidaria: Octocorallia) Iván Calixto-Botía1,2* and Juan A. Sánchez2,3 Abstract Background: Phenotypic plasticity, as a phenotypic response induced by the environment, has been proposed as a key factor in the evolutionary history of corals. A significant number of octocoral species show high phenotypic variation, exhibiting a strong overlap in intra- and inter-specific morphologic variation. This is the case of the gorgonian octocoral Antillogorgia bipinnata (Verrill 1864), which shows three polyphyletic morphotypes along a bathymetric gradient. This research tested the phenotypic plasticity of modular traits in A. bipinnata with a reciprocal transplant experiment involving 256 explants from two morphotypes in two locations and at two depths. Vertical and horizontal length and number of new branches were compared 13 weeks following transplant. The data were analysed with a linear mixed-effects model and a graphic approach by reaction norms. Results: At the end of the experiment, 91.8% of explants survived. Lower vertical and horizontal growth rates and lower branch promotion were found for deep environments compared to shallow environments. The overall variation behaved similarly to the performance of native transplants. In particular, promotion of new branches showed variance mainly due to a phenotypic plastic effect. Conclusions: Globally, environmental and genotypic effects explain the variation of the assessed traits. Survival rates besides plastic responses suggest an intermediate scenario between adaptive plasticity and local adaptation that may drive a potential process of adaptive divergence along depth cline in A. bipinnata. Keywords: Phenotypic plasticity, Antillogorgia bipinnata, Reaction norm, Octocoral, Depth cline Background will be hindered [2, 3]. However, the potential role of Phenotypic plasticity has been defined as the natural adaptive plasticity in promoting speciation has been capacity of an organism to react to a phenotypic change suggested in some cases where it can contribute to niche in form, state, movement or activity rate in response to diversification and further evolutionary change [1, 4–6]. environmental variation [1]. In the past century, pheno- Phenotypic and genetic accommodation, the Baldwin typic plasticity was largely considered a barrier to speci- effect, and the Waddington’s genetic assimilation have ation: if there is no need for genetic change to adapt to been proposed to explain environmental-induced changes the environment (masking the genotype for negative se- fixed in the genome and susceptible to promote a spe- lection), then the process of adaptive genetic divergence ciation process [7, 8]. Reciprocal transplant experiments consist of transfer- * Correspondence: [email protected] ring phenotypic variants to the opposite environments 1Department of Animal Ecology and Systematics, Justus Liebig Universität, and are a practical and cost-effective approach to testing Heinrich-Buff-Ring 26-32 IFZ D-35392, Giessen, Germany phenotypic plasticity. In marine systems, variation re- 2Laboratory of Biología Molecular Marina-Biommar, Department of Biological Sciences-Faculty of Sciences, Universidad de los Andes, Carrera 1E No 18A – lated to environmental heterogeneity has been specially 10, P.O. Box 4976, Bogotá, Colombia studied along depth gradients, which can vary in light Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Calixto-Botía and Sánchez BMC Evolutionary Biology (2017) 17:55 Page 2 of 8 intensity, wave exposure and nutrient concentration. In reassigned from the genus Pseudopterogorgia [19]. Popu- corals, most studies assessing plasticity and genetic lations of the complex A. bipinnata-kallos are clustered adaptation have found that adaptive divergence corre- in reefs in the Southern Caribbean, the Mesoamerican sponds to depth gradients. One of the first experiments Reef, with Panama and Belize populations closely related using a common garden approach on corals was done [20], and the Florida-Bahamas region. Colonies of the with Orbicella annularis and Siderastrea siderea, in four ‘deep’ morphotype are larger, with longer principal axes, reef habitats and detected high phenotypic plasticity in secondary branches, and internodal lengths, but fewer response to the transplanted habitat [9]. In another secondary branches in contrast to the ‘bushy’ morpho- study, shallow and deep morphotypes of Eunicea flex- type. These traits emerge from their modular organisa- uosa, a Caribbean gorgonian, exhibited low phenotypic tion, with the polyp as an iterative unit (sensu stricto) plasticity of sclerites and a strong genetic divergence sig- and branch as derived modular units [21, 22]. Thus, nal [10]. Finally, using reciprocal transplants of Seriato- differences in the architectural pattern between morpho- pora hystrix, a case of adaptive plasticity was detected in types shape the distribution and polyp density across the response to light conditions and adaptive divergence colony. Colony architecture has a feasible role in nutri- along the depth gradient [11, 12]. ent capture, overall photosynthetic rate, physical stress, Some Caribbean corals, including the feather-like and can be directly related to adaptive responses to en- gorgonian coral Antillogorgia bipinnata (Verrill 1864), vironmental variables in the depth cline. possess broad environmental preferences, sympatric dis- tributions, and contain highly plastic species complexes Study Area that are likely undergoing incipient ecological speciation The experiment was conducted at two localities in the processes [13–15]. A. bipinnata is distributed along northern Panamanian Caribbean, Hospital Point and coral reefs from 1 to 45 m deep in Panama, Belize, Crawl Key, Bocas del Toro (Fig. 1a). These locations ex- Bahamas, Florida, Colombia, but is absent on the hibit some environmental differences; Hospital Point is a Eastern side of the Western Atlantic. Along with this protected reef with abundant suspended particles and bathymetric gradient, the species varies phenotypically, low water motion compared to Crawl Key. 15 km away, including variation in size, coloration, sclerite form and Crawl Key is an exposed reef flat, characterised by branching pattern. Three basic morphotypes can be eroded coral skeletons and greater light penetration. recognised over a depth cline, the ‘deep morphotype’, Shallow habitats are characterised by coarser sand ‘typical morphotype’ and ‘bushy morphotype’ or ‘kallos’ with corals typically established on hard surfaces, such [15], the latter (A. kallos Bayer) described as a distinct as rocks. In contrast, in deep habitats, the slope is species [16, 17]. In some coral reefs (such as Panama) lower with greater sediment perturbation. Data for including at depths as shallow as 7 m, all three morpho- temperature and illuminance (total luminous flux per types can be present where there is an abrupt change in unit area) were collected using HOBO temperature depth and reef slope, suggesting that this physiological and light data loggers (Hobo Water Temp Pro, Onset challenge promotes an adaptive morphological response. Computer Corp., Bourne, Mass). In the shallow habi- To identify the contribution of plasticity to trait vari- tat at both localities, the temperature ranged between ation in corals emerging from the colonial structure, a 26–31 °C in comparison to 26–30 °C for deep habitats. reciprocal transplant experiment was carried out be- Illuminance strongly varied between habitats with the tween the deep and bushy morphotypes of A. bipinnata greatest variation in shallow habitats of Crawl Key (0– from two locations in Bocas del Toro, Panama. With this 35800 lux), and Hospital Point (0–30300 lux). In deep research, we measured modular traits related to habitats, illuminance varied from 0–14400 lux for bathymetric adaptation to detect the genotypic and en- Crawl Key and 0–2900 lux at Hospital Point. vironmental components involved in colonial structure variation between morphotypes of A. bipinnata. These Establishing reciprocal transplants and data collection data deepen our understanding of the evolutionary To assess the response of modular traits after transplant- mechanisms and patterns of diversification for a remark- ation, we took advantage of the overcompensation able number of species from this subclass that show phenomenon in A. bipinnata, a fast apical branching re- marked phenotypic variation related to environmental sponse following injury [23]. Fragments approximately gradients [17, 18]. 30 cm long were cut from 32 healthy colonies of
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