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Article (Refereed) - Postprint Article (refereed) - postprint Corrigan, Laura J.; Horton, Tammy; Fotherby, Heather; White, Thomas A.; Hoelzel, A. Rus. 2014 Adaptive Evolution of Deep-Sea Amphipods from the Superfamily Lysiassanoidea in the North Atlantic. Evolutionary Biology, 41 (1). 154-165. 10.1007/s11692-013-9255-2 © Springer Science+Business Media B.V. 2014 This version available at http://nora.nerc.ac.uk/506854/ NERC has developed NORA to enable users to access research outputs wholly or partially funded by NERC. Copyright and other rights for material on this site are retained by the rights owners. Users should read the terms and conditions of use of this material at http://nora.nerc.ac.uk/policies.html#access This document is the author’s final manuscript version of the journal article, incorporating any revisions agreed during the peer review process. Some differences between this and the publisher’s version remain. You are advised to consult the publisher’s version if you wish to cite from this article. The final publication is available at link.springer.com Contact NOC NORA team at [email protected] The NERC and NOC trademarks and logos (‘the Trademarks’) are registered trademarks of NERC in the UK and other countries, and may not be used without the prior written consent of the Trademark owner. 1 Adaptive Evolution of Deep-Sea Amphipods from the Superfamily 2 Lysiassanoidea in the North Atlantic 3 4 5 Laura J. Corrigan1, Tammy Horton2, Heather Fotherby1, Thomas A. White1 & A. Rus 6 Hoelzel1 7 8 1) School of Biological and Biomedical Sciences, Durham University, South Road, 9 Durham, DH1 3LE, UK 10 11 2) Ocean Biogeochemistry and Ecosystems, National Oceanography Centre, 12 University of Southampton, European Way, Southampton, SO14 3ZH, UK 13 14 Correspondence: A. Rus Hoelzel, School of Biological and Biomedical Sciences, 15 Durham University, South Road, Durham, DH1 3LE, UK; email: 16 [email protected]; phone: 0191-334-1200. 17 18 Keywords: amphipod, evolution, phylogenetics, adaptation, deep-sea 19 Abstract 20 21 In this study we reconstruct phylogenies for deep sea amphipods from the 22 North Atlantic in order to test hypotheses about the evolutionary mechanisms driving 23 speciation in the deep sea. We sequenced five genes for specimens representing 21 24 families. Phylogenetic analyses showed incongruence between the molecular data 25 and morphological taxonomy, with some morphologically distinct taxa showing close 26 molecular similarity. Approximate dating of nodes based on available calibration 27 suggested adaptation to the deep sea around the Cretaceous-Palaeogene boundary, 28 with three identified lineages within the deep-sea radiation dating to the Eocene- 29 Oligocene transition. Two of those lineages contained species currently classified in 30 multiple families. We reconstructed ancestral nodes based on the mouthpart 31 characters that define trophic guilds (also used to establish the current taxonomy), and 32 show a consistent transition at the earliest node defining the deep-sea lineage, together 33 with increasing diversification at more recent nodes within the deep-sea lineage. 34 The data suggest that the divergence of species was adaptive, with successive 35 diversification from a non-scavenging ancestor to ‘opportunistic’, ‘obligate’ and 36 ‘specialised’ scavengers. We propose that the North Atlantic species studied provide 37 a strong case for adaptive evolution promoted by ecological opportunity in the deep 38 sea. 39 40 Keywords: deep sea; amphipod; invertebrate; adaptation; phylogenetics 41 1. Introduction 42 It has been proposed that effectively continuous marine environments with 43 few obvious geographical barriers should allow broad dispersal and promote panmixia 44 (reviewed in Palumbi 1994), inhibiting reproductive isolation and speciation (known 45 as the ‘marine speciation paradox’; Bierne et al. 2003). There are two main 46 hypotheses generally put forward to explain the observed patterns of speciation in the 47 marine environment. One is that species divergence is the result of ecological 48 speciation (Puebla 2009) generating adaptive radiations, when multiple lineages 49 evolve from a single common ancestor at a rapid pace. The other involves 50 differentiation across geographic barriers which may include oceanographic factors 51 such as current systems or thermal fronts (though typically less clearly defined than 52 boundary systems in terrestrial environments). According to the first idea, relaxed 53 ecological constraints (abundant resources and reduced competition) may create 54 ecological opportunity in the colonisation of new habitats resulting in adaptive 55 divergence (Schluter 1996; Schluter 2000; Puebla 2009). For example, speciation in 56 the Pacific rockfish genus (Sebastes) is associated with divergence in habitat depth 57 and depth-associated morphology, in the absence of geographic barriers (Ingram 58 2011). 59 According to the second idea, tectonically-driven changes to ocean basins or 60 oceanographic factors may generate physical barriers to dispersal in vicariance events 61 resulting in allopatric or parapatric speciation (reviewed in Palumbi 1994). Fully 62 allopatric speciation has been observed across barriers such as the Isthmus of Panama 63 (e.g. Marko 2002) but such clear examples are relatively rare in the marine 64 environment. The same mechanisms that generate vicariance may generate ecological 65 opportunity by releasing habitat that can then be colonised. 66 Adaptive radiations can be difficult to identify, but should be characterised by 67 a correlation between phenotype and environment, novel phenotypes providing a 68 selective advantage (difficult to prove without experimentation), and speciation 69 should be rapid, with the emergence of multiple species from a recent common 70 ancestor (see Schluter 2002). They have been frequently described for terrestrial and 71 freshwater ecosystems, including well-known cases such as the Galapagos finches 72 (e.g Schluter & Grant 1984) and cichlids of the African rift lakes (e.g. Seehausen 73 2006). 74 In aquatic ecosystems, habitat shifts from marine to freshwater have been 75 shown to promote species diversification (e.g. Hou et al. 2011). Adaptive radiations 76 described for marine systems include reef fish (e.g. Taylor & Hellburg 2005; Puebla 77 2007) and Antarctic fish species (Clarke & Johnson 1996). However, habitat shifts 78 from shallow to deep-sea environments have been less well supported in the literature 79 (but see Distel et al. 2000). Historically, deep-sea environments were thought to 80 harbour reduced species diversity due to harsh environmental conditions (see Hessler 81 & Sanders 1967). It was further suggested that rates of evolution were much slower 82 at depth, leading to the idea that the deep sea was a refuge for ancient relics 83 (Zenkevitch & Birstein 1960). More recently however, greater species diversity has 84 been documented in various groups in the deep sea, including bivalves, gastropods, 85 polychaetes and isopod crustaceans (reviewed in Wilson & Hessler 1987; Grassle 86 1989). 87 Here we examine the phylogeny of deep-sea amphipods in order to investigate 88 the evolutionary processes driving their speciation in the deep sea. Amphipods 89 occupy almost all aquatic environments as well as some subterranean and terrestrial 90 habitats (Barnard & Karaman 1991). Despite their widespread distribution, the 91 relationships among and within the major amphipod taxonomic groups are poorly 92 resolved, possibly due to the effects of convergent evolution (Englisch et al, 2003; 93 Macdonald et al, 2005; Hou et al; 2007; Fiser et al, 2008; Ito et al, 2008; Havermans 94 et al, 2010). We focus our analysis on amphipods collected at our study sites at the 95 mid-Atlantic ridge, which can be classified within the superfamily Lysianassoidea 96 (the taxonomy of which remains controversial, see below). Lysianassoid amphipods 97 can be found from the colder waters of the Polar Regions (De Broyer et al., 2004) to 98 the tropics (Lowry & Stoddart, 2009) and from the intertidal to the deepest ocean 99 trenches (Jamieson et al., 2010). Many members of the Lysianassoidea are known to 100 be epibenthic, and infaunal scavengers and carnivores. They are numerically and 101 taxonomically the most important group of deep-sea scavengers (Wolff, 1970; Hessler 102 et al., 1978; Smith, 1985; Thurston, 1990). 103 There have been numerous studies of the amphipod scavenging fauna in the 104 deep sea, including biodiversity, distribution, ecology, taxonomy, and respiration and 105 pressure effects (e.g. Hargrave, 1985; De Broyer, 2004; Premke & Graeve, 2009; 106 Thurston 1979; 1990). However, despite the fact that the group contains some of the 107 most primitive amphipods (Bousfield & Shih, 1994), little attention has been paid to 108 studies of the molecular phylogeny of this group, and the Amphipoda in general have 109 a history of taxonomic instability in the higher ranks (Superfamily and higher) to the 110 extent that that they are generally listed alphabetically (e.g. see Martin & Davis, 111 2001). However, a recent study by Havermans et al (2010), looked at the molecular 112 phylogeny of Antarctic lysianassoids in the families, Lysianassidae and Uristidae, 113 based on nuclear 28S rRNA and mitochondrial cytochrome oxidase subunit I genes, 114 and showed that the molecular and morphological taxonomies of these groups are 115 largely incongruent and did not support the monophyly of several of the currently 116 proposed
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