Allopatric and Sympatric Drivers of Speciation in Alviniconcha Hydrothermal Vent Snails
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University of Rhode Island DigitalCommons@URI Graduate School of Oceanography Faculty Publications Graduate School of Oceanography 7-2020 Allopatric and Sympatric Drivers of Speciation in Alviniconcha Hydrothermal Vent Snails Corinna Breusing University of Rhode Island, [email protected] Shannon B. Johnson Verena Tunnicliffe David A. Clague Robert C. Vrijenhoek See next page for additional authors Follow this and additional works at: https://digitalcommons.uri.edu/gsofacpubs Citation/Publisher Attribution Corinna Breusing, Shannon B Johnson, Verena Tunnicliffe, David A Clague, Robert C Vrijenhoek, Roxanne A Beinart, Allopatric and Sympatric Drivers of Speciation in Alviniconcha Hydrothermal Vent Snails, Molecular Biology and Evolution, Volume 37, Issue 12, December 2020, Pages 3469–3484, https://doi.org/10.1093/molbev/msaa177 This Article is brought to you for free and open access by the Graduate School of Oceanography at DigitalCommons@URI. It has been accepted for inclusion in Graduate School of Oceanography Faculty Publications by an authorized administrator of DigitalCommons@URI. For more information, please contact [email protected]. Authors Corinna Breusing, Shannon B. Johnson, Verena Tunnicliffe, David A. Clague, Robert C. Vrijenhoek, and Roxanne A. Beinart This article is available at DigitalCommons@URI: https://digitalcommons.uri.edu/gsofacpubs/752 Allopatric and Sympatric Drivers of Speciation in Alviniconcha Hydrothermal Vent Snails Corinna Breusing ,*‡,1 Shannon B. Johnson,‡,2 Verena Tunnicliffe,3 David A. Clague,2 Robert C. Vrijenhoek,2 and Roxanne A. Beinart1 1Graduate School of Oceanography, University of Rhode Island, Narragansett, RI 2Monterey Bay Aquarium Research Institute, Moss Landing, CA 3Department of Biology and School of Earth and Ocean Sciences, University of Victoria, Victoria, BC, Canada †These authors contributed equally to this work. *Corresponding author: E-mail: [email protected]. Associate editor: Li Liu New Sanger sequences for Alviniconcha and Ifremeria hosts and symbionts are available in GenBank under accession numbers Downloaded from https://academic.oup.com/mbe/article/37/12/3469/5870836 by guest on 14 January 2021 MT131487–MT131781 (COI), MT130994–MT131149 (12S), MT146898–MT147385 (H3), MT148092–MT148633 (ATPSa), MT148634–MT149209 (ATPSb), MT147386–MT148091 (EF1a), and MT137388–MT137420 (16S). 16S amplicon sequences have been deposited in the Sequence Read Archive under BioProject numbers PRJNA473256, PRJNA473257, PRJNA610289, and PRJNA610290. Abstract Despite significant advances in our understanding of speciation in the marine environment, the mechanisms un- derlying evolutionary diversification in deep-sea habitats remain poorly investigated. Here, we used multigene molecular clocks and population genetic inferences to examine processes that led to the emergence of the six extant lineages of Alviniconcha snails, a key taxon inhabiting deep-sea hydrothermal vents in the Indo-Pacific Ocean. We show that both allopatric divergence through historical vicariance and ecological isolation due to niche segregation contributed to speciation in this genus. The split between the two major Alviniconcha clades (separating A. boucheti and A. marisindica from A. kojimai, A. hessleri, and A. strummeri) probably resulted from tectonic processes leading to geographic separation, whereas the splits between co-occurring species might have been influenced by ecological factors, such as the availability of specific chemosynthetic symbionts. Phylogenetic origin of the sixth species, Alviniconcha adamantis, remains uncertain, although its sister position to other extant Alviniconcha lineages indicates a possible ancestral relationship. This study lays a foundation for future genomic studies aimed at deciphering the roles of local adaptation, reproductive biology, and host–symbiont compatibility in speciation of these vent-restricted snails. Key words: Alviniconcha, speciation, allopatric divergence, ecological isolation, deep-sea hydrothermal vents, chemo- Article synthetic symbionts. Introduction ecological niches (Rundle and Nosil 2005; Schluter 2009). Habitat isolation can occur at different spatial scales that How novel species evolve in response to environmental range from “macrospatial” (a form of allopatric speciation, pressures remains a fundamental question in evolutionary where gene flow between populations is absent due geo- biology (Schluter 1998). New species can originate through a graphic separation) to “microspatial” (where distinct popu- number of mechanisms, including geographic isolation (al- lations co-occur geographically but rarely interbreed lopatric speciation) and formation of reproductive barriers because of adaptations to different ecological niches) due to localized natural selection (sympatric speciation) (Coyne and Orr 2004). By contrast, mutation-order specia- (Darwin 1859; Mayr 1942; Dobzhansky 1951; Coyne and tion happens when reproductive isolation evolves due to Orr 2004; Schuler et al. 2016; Yang et al. 2017). The evolution random fixation of alleles in two populations that face the of new species commonly occurs as a result of ecological or same selective pressures (Mani and Clarke 1990; Schluter mutation-order speciation (Schluter 2009). Ecological speci- 2009; Nosil and Flaxman 2011). Evolutionary divergence un- ation theory predicts that reproductive isolation should der this scenario is unlikely (though not impossible) if gene evolve between populations adapting to different environ- flow is present (Schluter 2009; Nosil and Flaxman 2011), ments (Mayr 1942) and is a consequence of divergent selec- whereas ecological speciation is common with or without tion on functional traits enabling specialization for distinct gene flow (Schluter 2009; Nosil and Flaxman 2011; Feder ß The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Open Access Mol. Biol. Evol. 37(12):3469–3484 doi:10.1093/molbev/msaa177 Advance Access publication July 13, 2020 3469 Breusing et al. doi:10.1093/molbev/msaa177 MBE et al. 2012; Campbell et al. 2018). Additional processes in- Alviniconcha and Ifremeria are nutritionally dependent on cluding inter-specific hybridization and host–microbe asso- horizontally transmitted, chemosynthetic sulfide-oxidizing ciations have received less attention but are now accepted endosymbionts that are acquired from a diverse community as significant drivers of speciation (Schuler et al. 2016). of environmental bacteria and are harbored within vacuoles Our current understanding of speciation mechanisms in the gill filaments (Windoffer and Giere 1997; Suzuki, Sasaki, in animals stems mostly from evolutionary research on ter- Suzuki, Nogi, et al. 2006; Trembath-Reichertetal.2019). restrial and freshwater organisms, whereas less is known Except for A. boucheti and A. marisindica,whicharecon- about speciation in oceanic environments, in particular strained to symbionts of the class Campylobacteria (formerly deep ocean basins (Miglietta et al. 2011). Processes that Epsilonproteobacteria; Waite et al. 2017), all other lead to evolutionary divergence in marine systems may differ Alviniconcha species and Ifremeria nautilei typically host from other environments given that physical barriers are less Gammaproteobacteria symbionts (Urakawa et al. 2005; pronounced and deep-sea habitats might have been less af- Suzuki, Sasaki, Suzuki, Nogi, et al. 2005;Suzuki,Sasaki, fected by past climatic fluctuations (Miglietta et al. 2011;but Suzuki, Tsuchida, et al. 2005; Suzuki, Kojima, Sasaki, et al. Downloaded from https://academic.oup.com/mbe/article/37/12/3469/5870836 by guest on 14 January 2021 see Vrijenhoek 2013), at least over much of the Cenozoic. 2006; Suzuki, Kojima, Watanabe, et al. 2006; Beinartetal. Nonetheless, deep-sea hydrothermal vents provide an excep- 2012). In zones of sympatry, the two snail genera occupy tion to other deep-sea environments due to their global but relatively narrow ranges of chemical and thermal conditions that are well within their physiological tolerance limits and island-like distribution and their relative instability on ecolog- that do not support maximal rates for chemoautotrophic ical and geological time scales (Vrijenhoek 2013). The dense growth (Sen et al. 2013). This observation suggests that inter- animal communities living in these habitats are exposed to species competition is an important factor determining the highly variable and extreme environmental conditions, and realized niche of these snails (Sen et al. 2013). Beinart et al. many of the invertebrates are sustained through obligate (2012) proposed that host niche utilization is strongly influ- symbiosis with chemosynthetic bacteria (Dubilier et al. enced by the availability and metabolic capacity of locally dom- 2008). The phylogenetically and ecologically closely related inant symbiont phylotypes. In their study of co-occurring snail genera Alviniconcha and Ifremeria (Gastropoda: Alviniconcha species from the Lau Basin, they showed that Abyssochrysoidea) are among the dominant inhabitants of the distribution and abundance of host–symbiont combina- Indo-Pacific hydrothermal vents. The genus Ifremeria is tions (holobionts) followed