Phylogeny and Habitat-Use of Ampharetidae (Annelida, Terebelliformia) in Chemosynthesis-Based Ecosystems Mari H

Eilertsen et al. BMC Evolutionary Biology (2017) 17:222 DOI 10.1186/s12862-017-1065-1 RESEARCHARTICLE Open Access Do ampharetids take sedimented steps between vents and seeps? Phylogeny and habitat-use of Ampharetidae (Annelida, Terebelliformia) in chemosynthesis-based ecosystems Mari H. Eilertsen1,2* , Jon A. Kongsrud3, Tom Alvestad3, Josefin Stiller4, Greg W. Rouse4 and Hans T. Rapp1,2,5 Abstract Background: A range of higher animal taxa are shared across various chemosynthesis-based ecosystems (CBEs), which demonstrates the evolutionary link between these habitats, but on a global scale the number of species inhabiting multiple CBEs is low. The factors shaping the distributions and habitat specificity of animals within CBEs are poorly understood, but geographic proximity of habitats, depth and substratum have been suggested as important. Biogeographic studies have indicated that intermediate habitats such as sedimented vents play an important part in the diversification of taxa within CBEs, but this has not been assessed in a phylogenetic framework. Ampharetid annelids are one of the most commonly encountered animal groups in CBEs, making them a good model taxon to study the evolution of habitat use in heterotrophic animals. Here we present a review of the habitat use of ampharetid species in CBEs, and a multi-gene phylogeny of Ampharetidae, with increased taxon sampling compared to previous studies. Results: The review of microhabitats showed that many ampharetid species have a wide niche in terms of temperature and substratum. Depth may be limiting some species to a certain habitat, and trophic ecology and/or competition are identified as other potentially relevant factors. The phylogeny revealed that ampharetids have adapted into CBEs at least four times independently, with subsequent diversification, and shifts between ecosystems have happened in each of these clades. Evolutionary transitions are found to occur both from seep to vent and vent to seep, and the results indicate a role of sedimented vents in the transition between bare-rock vents and seeps. Conclusion: The high number of ampharetid species recently described from CBEs, and the putative new species included in the present phylogeny, indicates that there is considerable diversity still to be discovered. This study provides a molecular framework for future studies to build upon and identifies some ecological and evolutionary hypotheses to be tested as new data is produced. Keywords: Ampharetidae, Annelida, Chemosynthesis-based ecosystems, Deep-sea, Evolutionary stepping-stones, Phylogeny, Sedimented vents, Specialization * Correspondence: [email protected] 1Department of Biology, University of Bergen, Bergen, Norway 2K.G. Jebsen Centre for Deep-Sea Research, University of Bergen, Bergen, Norway 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. Eilertsen et al. BMC Evolutionary Biology (2017) 17:222 Page 2 of 15 Background from sedimented vents and one species is also recorded In the deep-sea, there is no sunlight to fuel photosynthetic from the Costa Rica hydrothermal seep [23–25]. Although primary production. Energy to sustain life is therefore either some species of ampharetids encountered in CBEs are also derived from organic matter falling from surface waters, or found in the surrounding deep-sea [29], many species are from chemosynthetic primary production. Chemosynthetic exclusively known from CBEs and are considered to be bacteria and archaea, which utilize energy from reduced specialists [23–27]. Ampharetids are deposit feeders, and chemical compounds (e.g. hydrogen sulfide or methane) in- gut content, fatty acid and isotope analyses indicate that stead of sunlight, are found both free-living and as symbi- specialized ampharetids in CBEs are feeding on chemosyn- onts of macrofauna [1]. Compared to the surrounding food- thetic bacteria [2, 30–32]. Most ampharetids are habitat- limited deep-sea, chemosynthesis-based ecosystems (CBEs) specific, and even when hydrothermal vents and cold seeps are teeming with macrofauna, and specialized organisms are found in close geographic proximity, the same species can reach extremely high population densities (e.g. [2]). of ampharetids are usually not found in both habitats [25]. Three main categories of deep-sea CBEs are defined The almost ubiquitous presence of ampharetids in various based on the process that forms the reduced chemical CBEs makes them a good model taxon to study the evolu- compounds: hydrothermal vents, cold seeps and organic tion of habitat-use in heterotrophic animals. falls [3]. However, there are some habitats that have been Although Ampharetidae is one of the most common considered intermediates between vents and seeps, such as groups within CBEs, only two molecular phylogenies have sedimented vents [4] and hydrothermal seeps [5], and re- been published to date, both with a limited taxon sampling cent work has suggested that CBEs form a continuum of of the family [23, 25]. The first study by Stiller et al. [25] fo- environmental conditions [5–7]. Some animal clades are cused on the genus Amphisamytha, which has 7 recognized shared across vents, seeps and falls, which demonstrates species from vent and seep habitats. The second phylogeny the evolutionary link between these habitats [8], but on a by Kongsrud et al. [23] included five additional species from global scale the number of shared species is low [3, 4, 9]. In CBEs belonging to the genera Pavelius, Paramytha and addition to the geochemical differences between CBEs, the Grassleia and indicated that adaptation into CBEs has hap- distinctiveness of the fauna is affected by the geographic pened multiple times independently in Ampharetidae, but proximity of habitats [6, 10], and differences in depth [10, still with limited taxon sampling of non-CBE ampharetids. 11] and substratum [6, 7]. In the Guaymas Basin, where In this paper, we expanded upon previous efforts and sedimented vents and seeps are found in close geographic present a multi-gene phylogeny with increased taxon proximity and at similar depth, the macrofaunal commu- sampling of species both from CBEs and other habitats. In nity composition is not determined by the type of ecosys- addition, we performed a review of the habitat-use of CBE- tem, but rather by environmental parameters that vary specialized ampharetids. With this we aimed to: 1) assess across ecosystems [6]. Similarly, no clear distinction was the effect of environmental factors such as substratum, found between sedimented vents in Okinawa Trough and temperature and depth on the habitat-specificity and distri- seeps at similar depths in Sagami Bay [10]. Recently, a bio- butions of ampharetids in CBEs; 2) test the hypothesis of geographic analysis demonstrated the importance of sedi- multiple evolutionary origins of ampharetids in CBEs; and mented vents in linking vent and seep faunas on a global 3) infer the frequency and direction of habitat-shifts in the scale, and also indicated that sedimented vents might have evolutionary history of Ampharetidae, with special atten- been central in the evolution of taxa within CBEs [7]. tion paid to the role of intermediate habitats such as sedi- Over the last decades, a number of phylogenetic studies mented vents and hydrothermal seeps. have elucidated the evolutionary histories of fauna from CBEs, but these have mostly focused on the dominant Methods symbiotrophic taxa such as vesicomyid and bathymodiolin Review of habitat use bivalves [12–16] and siboglinid annelids [17–19]. The hy- For the review we only included species of Ampharetidae pothesis that vent and seep mussels (Bathymodiolinae) obligate to CBEs. Although molecular data indicates that evolved from wood-dwelling ancestors [20] has been Alvinellidae should be considered a subfamily of Amphare- followed by studies on other taxa, with either organic falls tidae ([25], present study), species in this group were not or seeps functioning as stepping-stones into the vent habi- included in the review due to their unique and very special- tat [14, 15, 18, 21, 22]. However, the role of sedimented ized ecology [33]. Because of the difficulty in validating re- vents as an evolutionary stepping-stone has not previously cords of species that are not formally described (recorded been assessed in a phylogenetic framework. as genus sp. nov.), we further limited the review to species Ampharetidae is a commonly occurring taxon at hydro- that are formally described, plus the undescribed species in- thermal vents [23–26], cold seeps [2, 24, 26] and organic cluded in the present phylogeny (23 species in total). Details falls [27, 28] and can be a dominant part of the macrofau- of the habitat where the specimens were collected are often nal community [2, 4]. There are several species described not included in published papers, therefore cruise reports Eilertsen et al. BMC Evolutionary Biology (2017) 17:222 Page 3 of 15 were also studied when these were available [34]. For each 25 μl. For the remaining specimens, the PCR reactions were record, we collected data on: habitat (hydrothermal vent, set up as in [23]. The PCR cycling profile for 28S for all spec- sedimented vent, inactive vent, hydrothermal seep, cold imens was as follows: 3 min at 94 °C, 7 cycles with 30 s at seep or organic fall), temperature, water/fluid chemistry, 94 °C, 30 s at 55 °C and 2 min at 72 °C, 35 cycles with 30 s depth, substratum and geographical locality. All literature at 94 °C, 30 s at 52 °C, and 2 min at 72 °C, and finally included in the review can be found in Additional file 1.

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