Department of Biology ......Convergent evolution and associated character homoplasy are one of the...

Phylogenetic analysis of lineage relationships among hyperiidamphipods as revealed by examination of the mitochondrial gene,cytochrome oxidase I (COI)William E. Browne,1,* Steven H. D. Haddock,† and Mark Q. Martindale1

*Kewalo Marine Lab, Pacific Biosciences Research Center, University of Hawaii, 41 Ahui St Honolulu, HI 96813, USA;†Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA

Synopsis Among metazoans, crustaceans display the greatest disparity between body plans and are second only to the

insects in overall species diversity. Within the crustaceans, the Amphipoda rank as one of the most speciose extant orders.

Amphipods have successfully invaded a variety of ecosystems, including the pelagic midwater environment. Despite their

abundance in varied and dissimilar habitats, and the use of traditional morphological and systematic comparative

analyses, phylogenetic relationships among amphipods remain uncertain. The pelagic amphipods, hyperiids, have highly

divergent life histories and morphological attributes in comparison to more familiar benthic, nearshore, intertidal, and

terrestrial amphipods. Some of these adaptations are likely correlated with their pelagic life history and include features

such as hypertrophied olfactory and visual systems, duplications of the eyes, and an array of modifications to the

appendages. Many of these morphological features may represent homoplasies, thus masking the true phylogenetic

relationships among extant hyperiid amphipods. Here, we sample a wide range of amphipod taxa for the COI gene and

present the first preliminary molecular phylogeny among the hyperiids.

Introduction

Amphipoda [Crustacea; Malacostraca; Peracarida]is a monophyletic, species-rich, assemblage (Schram1986; Schmitz 1992). They occur in nearly all knownmarine, freshwater, and brackish water environmentsas well as in highly humid terrestrial ecosystems(Barnard and Karaman 1991; Van Dover 1992;Vinogradov et al. 1996; Poltermann et al. 2000;Takhteev 2000; Serejo 2004). This ecological diversityis reflected in similarly high levels of morphologicalvariation. The unique structure and arrangementof the posterior-most three pairs of appendages(uropods) represent the exclusive, synapomorphic,characters that unite the amphipods as a natural,monophyletic group. They are further distinguishedby a combination of additional features includinglateral compression of the body, presence of sessilecompound eyes, the general orientation of thethoracomere appendages (pereopods) to the bodyaxis, and the close arrangement of the anteriorgnathal appendages, including the maxillipeds, intoa basket-like shape around the mouth to form acompact buccal mass. The amphipods have tradi-tionally been organized into four groups, the largely

benthic taxa Gammaridea, Caprellidea, Ingolfiellidea,and the exclusively pelagic midwater taxonHyperiidea (Martin and Davis 2001). The pelagichyperiid amphipods are a major constituent ofcrustacean zooplankton (Bowman and Gruner1973) and in some regions their swarming behaviorleads to their being a primary food source for largeplanktivores (Vinogradov et al. 1996).

The phylogenetic relationships among the hyper-iids remain a mystery. In fact, the relationshipsamong, and within, all four of the major amphipodtaxonomic groups remain poorly resolved due toconflicting suites of morphological characters cur-rently in use by systematists (Martin and Davis2001). This presents a conundrum in which we haveno large-scale phylogenetic hypotheses for theAmphipoda, a highly successful monophyleticgroup that has high biological diversity coupledwith evolutionary radiations in dissimilar environ-ments. Although there have been recent advances inmorphological and molecular analyses among someof the gammaridean groups of amphipods (Meyranet al. 1997; Englisch et al. 2003; Myers and Lowry2003; Lorz and Held 2004; Serejo 2004; Davolos andMaclean 2005; Macdonald et al. 2005), there have

From the symposium ‘‘Integrative Biology of Pelagic Invertebrates’’ presented at the annual meeting of the Society for Integrative andComparative Biology, January 3–7, 2007, at Phoenix, Arizona.1E-mail: [email protected]

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Integrative and Comparative Biology, volume 47, number 6, pp. 815–830doi:10.1093/icb/icm093Advanced Access publication October 30, 2007! The Author 2007. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.For permissions please email: [email protected].

been no molecular phylogenetic studies and fewcomparative morphological analyses among thehyperiids (Pirlot 1932; Coleman 1994; Zeidler 1999,2003a, 2003b, 2004). This is surprising given thatmany descriptions of hyperiid species date from the19th century and nearly all midwater plankton tows,at any depth, recover representatives from the group.Some of the major biological and evolutionaryquestions that rely on a hypothesis of lineagerelationships, and thus remain unaddressed in thisgroup include how patterns of biological diversityarise, how biological form and function are linked toevolutionary radiations, and in the particular case ofthe pelagic hyperiids, what aspects of their body planare required for successful colonization and radiationwithin midwater niches. Phylogenetic analysis canultimately address whether an ancestral benthicamphipod stem group invaded the pelagos, orconversely, whether an ancestral pelagic amphipodstem group invaded the benthos, or whether therehas been a more complex interplay between hyperiidlineages with regard to colonization of oceanicmidwater habitats.

An accurate phylogenetic assessment using purelymorphological features is problematic. Thus far,there is no single synapomorphy known for thehyperiids. As a consequence the notion of hyperiidpolyphyly has been suggested in some of the majortaxonomic works (reviewed by Vinogradov et al.1996). This suggests extensive convergence, orhomoplasy, of groups of morphological attributesrequired for a pelagic existence and for theirfrequently observed associations with gelatinouszooplankton.

Convergent evolution and associated characterhomoplasy are one of the central themes in evo-lutionary biology and arguably one of the mostdifficult problems facing phylogenetic reconstructionof relationships within and among lineages.Character homoplasy can easily mask relationshipsbetween related lineages (examples among amphi-pods include structural simplifications such asreductions of the maxilliped, the pleopods, and theuropods). Environmental factors play a strong role inthe evolutionary shaping of morphologies throughtime. Since all hyperiid taxa are pelagic, it isinstructive to consider some of the major featuresaffecting organisms in the marine midwater environ-ment. Volumetrically, the oceanic midwater ismassive, accounting for !90–99.8% of the habitablespace on the planet (Cohen 1994). Although vast,the oceanic midwater environment is far from beingfeatureless and many biologically relevant partitions

can, and should be, taken into account whenconsidering organismal diversity in the midwater.

One of the most critical parameters affectingmidwater organisms is light (reviewed by Warrantand Locket 2004). The average depth of the openocean is 3800m. Down-welling ambient light (sun,moon, and starlight) penetrates as deep as 1000m.Long wavelength light is rapidly absorbed within thefirst !150m of the water column, the epipelagiczone, leaving only shorter wavelength light toilluminate the mesopelagic zone (!150–1000mdepth). The remaining !75% of midwater habitat,the bathypelagic (!1000–2500m depth) and abysso-pelagic (!2500m depth and beyond) zones, ischaracterized by an absence of down-welling surfacelight. In the bathypelagic and abyssopelagic zonesdown-welling light is completely replaced by omni-directional bioluminescent point light sources. Manyhyperiids participate in well-characterized cyclical,vertical, diel migrations driven by light, in whichzooplankton move upward in the water column atdusk and downward at dawn. This includes manyhyperiid species described as being associated withthe mesopelagic and bathypelagic midwater zones(Vinogradov et al. 1996). Two additional biologicallyimportant parameters of consequence at mesopelagic,bathypelagic, and abyssopelagic depths are dissolvedoxygen content and temperature. Between 400 and1000m is an oxygen poor water layer of variablethickness, the hypoxic oxygen minimum layer(OML), a niche in which there are particularadaptations such as reduced metabolic rates,improved oxygen uptake, and increased dependenceon anaerobic metabolism (Childress and Seibel1998). Additionally, these depths are characterizedby constant temperatures near 48C.

Another significant physical attribute of the mid-water environment is its inherent patchiness. Thispatchiness, or granularity, creates substantial 3Dsurfaces with which small clinging planktonicorganisms, in particular, can interact. This patchinessis a combination of both the planktonic organismsthemselves, as well as a host of other organicaggregates collectively known as ‘‘marine snow’’(Silver et al. 1978; Robison et al. 2005). Among theAmphipoda, modifications of morphologies asso-ciated with a clinging benthic life style could play arole in exploiting the variety of 3D surfaces presentin midwater habitats (Laval 1980).

The exclusively pelagic life style of the hyperiidshas historically made detailed studies of theseamphipods difficult. As in situ observations ofhyperiids continue to emerge, it is clear that mostspecies have complex life histories involving obligate

816 W. E. Browne et al.

commensalism or parasitic relationships with a widevariety of midwater gelatinous zooplankton such assiphonophores, salps, ctenophores, and cnidarians(Harbison et al. 1977; Madin and Harbison 1977;Harbison et al. 1978; Laval 1980; Gasca and Haddock2004; Gasca et al. 2007). Thus, the availability ofsurfaces in midwater appears to play an importantecological role among hyperiid amphipods andmorphological specializations in different hyperiidlineages may derive from interactions with preferredsurfaces.

We have used recent advances in SCUBA technol-ogy and modern techniques for collecting inmidwater in combination with traditional nettingto sample a diversity of hyperiid amphipods forthe mitochondrial gene, cytochrome oxidase I (COI),for a preliminary molecular assessment of hyperiidphylogenetic relationships. COI encodes for a sub-unit of cytochrome oxidase, an enzymatic proteincomplex absolutely required for aerobic metabolism(Castresana et al. 1994). COI was chosen forpreliminary analysis for several reasons includingmaternal inheritance of the mitochondrial genome,reduced occurrence of mitochondrial gene recombi-nation, extensive use of COI in phylogeneticreconstructions, and the availability of relatedsequences from publicly curated databases (Avise1986; Avise et al. 1987; Simon et al. 1994; Simonet al. 2006).

Materials and methods

Specimen collection

Amphipod specimens were collected using a varietyof techniques. Intertidal amphipods were collected byhand. Sub-surface benthic amphipods were collectedvia snorkeling, open-circuit (OC), and closed-circuitrebreather (CCR) SCUBA (Ambient Pressure DivingLtd., UK). Pelagic amphipods were collected using acombination of snorkeling, OC, and CCR SCUBAblue-water diving (Hamner 1975; Hamner et al.1975; Haddock and Heine 2005), remotely operatedunderwater vehicles (MBARI), ring nets, andopening-closing trawling nets (Childress et al.1978). Physical vouchers exist for all specimens andare housed at the Kewalo Marine Lab (Honolulu, HI,USA). Specimens of Parhyale hawaiensis came from abreeding colony maintained at the Kewalo MarineLaboratory (Browne et al. 2006) and those of Jassaslatteryi came from a breeding colony maintained atthe University of California at Berkeley (Patel).Specimens of hyperiid amphipods were identifiedusing the taxonomic keys of Bowman and Gruner(1973), Vinogradov et al. (1996), and Zeidler

(1999, 2003a, 2003b, 2004). Thirteen samplesincluded in this analysis were not identified tospecies level. They have been assigned temporarynames indicating their affinity to described species.

Sequence cloning

Genomic DNA was isolated with DNeasy Tissue Kit(Qiagen, Inc.) from isolated pleopod and/or dis-sected and isolated trunk muscle tissue. COI PCRwas completed using conserved primers LCO14905-GGT CAA CAA ATC ATA AAG ATA TTG G-3and HCOoutout 5-GTA AAT ATA TGR TGD GCTC-3 (Folmer et al. 1994; Schwendinger and Giribet2005). PCR products of the appropriate size weredirect sequenced by Macrogen, Inc (South Korea).

Phylogenetic analysis

Relevant COI sequences from 94 gammarids and twoisopod outgroups were selected and added to theanalysis from Genbank. Sequences were initiallyaligned and edited using Sequencher (Gene CodesCorporation). Multiple sequence alignments weregenerated using T-Coffee (Notredame et al. 2000).Alignments were then manually viewed and adjustedin MacClade v4.08 (Maddison and Maddison 2005).

Bayesian phylogenetic inference analysis wasexecuted with MrBayes 3.1.2 (Ronquist andHuelsenbeck 2003). The molecular evolution model,GTR"I"!, was selected using the AkaikeInformation Criterion (AIC) as implemented inModel-Test 3.7 (Posada and Crandall 1998). Fourindependent searches were run from 30 milliongenerations to 40 million generations, and trees weresampled every 100 generations. Likelihoods werevisualized with Tracer v1.3 (Rambaut andDrummond 2003) to determine the number ofgenerations to burn-in and to assess convergence ofdata sets. Consensus trees from the independent runswere compared to assess convergence and topologycongruence of data sets. A consensus tree from thecombined Bayesian runs was constructed andrepresents a total of 130 million generations fromthe four independent runs with trees sampled every1000 generations and an initial burn-in of 5 milliongenerations. Consensus trees were rooted with theisopod Armadillidium vulgare COI sequence.Resulting trees were visualized with TreeView X(Page 1996) and FigTree (http://evolve.zoo.ox.ac.uk/software.html?id#figtree).

Maximum likelihood (ML) analysis was executedwith RAxML-VI-HPC (Stamatakis 2006). The modelGTRMIX was selected for executing four initial runs,each with 250 searches. Searches from the ML runs

Lineage relationships among hyperiid amphipods 817

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were combined and the consensus from the top500 trees was visualized to assess convergenceof topologies. Bootstrapping of ML analysis wasexecuted with Seqboot (Felsenstein 1989) followed by20 independent searches for the most likely tree perbootstrap iteration with RAxML-VI-HPC. The besttree was retained for each of the 129 iterationsthat were executed. Resulting trees were visualizedwith FigTree (http://evolve.zoo.ox.ac.uk/software.html?id#figtree).

A mutational saturation plot (Philippe et al. 1994;Philippe and Forterre 1999) was generated using amaximum parsimony (MP) analysis with 10 randomsequence addition MP heuristic searches. The besttree was used to generate a patristic distance matrix.Individual pair-wise values were compared on X–Yscatter plots. The X-axis was used for the inferredsubstitution values and the Y-axis was used for theobserved substitution values.

Results

Phylogenetic analysis

A diversity of amphipods from the Northeast,Northwest, and Central Pacific, the western edgeof the Atlantic Gulf Stream, the Caribbean Sea,Germany, and the Weddell Sea were collected andsampled for !815 bp of the COI gene (Fig. 1,Table 1). The 72 new amphipod COI sequences

obtained for this study have been deposited withGenbank (Table 1). In an effort to test the hyperiidsas a monophyletic group within Amphipoda, addi-tional nonhyperiid amphipod COI sequences avail-able from Genbank were incorporated into ourphylogenetic analyses (Table 2). Our COI analysisincluded 168 taxa of which 52 represent a broadsampling among known hyperiidean forms.

Bayesian phylogenetic inference was used to inferCOI gene lineage relationships. The number ofgenerations required to stability (burn-in) was ashigh as 4.2 million, with an average burn-in of 3.5million generations across four independent runs.This was due, in part, to the large number of taxaanalyzed. Our combined bayesian COI analysisrecovered three clades of hyperiid amphipods(Figs. 2 and 4, Supplementary data). The hyperiidscomprising clade 1 appear to branch early among thetaxa included in this analysis. However, the relation-ship between hyperiids comprising clades 2 and 3, asdefined in this analysis, remain unclear. Althoughindependent runs always recovered the same topol-ogies among hyperiid taxa within each of the threeclades, the relationship between clade 2 and clade 3varied. The clade 2 hyperiids alternate between sisterto clade 3 hyperiids (Supplementary data) and sisterto the iphimediid gammarid clade (Supplementarydata); however, in both cases the resolution at thesedeep nodes is low. ML was also used to infer COI

Fig. 1 Map of localities at which collections were made. Black circles indicate areas from which amphipods were collected for the

present study (data appear in Table 1).


http://evolve.zoo.ox.ac.uk/software

Table 1 List of specimens collected

Taxon Collection Locality Latitude Longitude Depth (m) COI Accession

Acanthoscina acanthodes Fort Pierce, FL, USA 27.348N 79.548W 0–100 EF989700

Brachyscelus crusculum Kona coast, HI, USA 19.428N 156.078W 0–1 EF989658

Brachyscelus globiceps Kona coast, HI, USA 19.358N 156.008W 0–1 EF989660

Brachyscelus rapax Green Bay, PAN 9.148N 82.148W 0–2 EF989659

Calamorhynchus pellucidus Oahu, HI, USA 21.128N 158.198W 0–77 EF989649

Capprelid KBH Kewalo Basin Harbor 21.178N 157.518W 0–1 EF989681

Cilicaea sp. Kewalo Basin Harbor 21.178N 157.518W 0–1 EF989646

Cranocephalus scleroticus Kona coast, HI, USA 19.358N 156.008W 0–1 EF989648

Cyllopus lucasii Weddell Sea 60.948S 53.128W 0–353 EF989691

Cyllopus magellanicus Weddell Sea 60.948S 53.128W 0–353 EF989690

Cyphocaris sp. California, USA 36.338N 122.908W 300–700 EF989702

Cystisoma gershwinae California, USA 36.588N 122.508W 1144 EF989675

Cystisoma pellucida California, USA 36.438N 124.078W 0–400 EF989676

Gammarid KML KML seatables 21.178N 157.518W N/A EF989703

Gammarid Tib750 California, USA 36.268N 122.598W 2764 EF989706

Gammarid Tib844 California, USA 35.508N 123.878W 3591 EF989707

Glossocephalus milneedwardsi Pelican Cayes, BZ 16.408N 88.118W 0–3 EF989654

Glossocephalus sp California, USA 36.608N 122.378W 541 EF989655

Hyperia macrocephala Weddell Sea 60.568S 52.818W 0–328 EF989666

Hyperietta parviceps Kona coast, HI, USA 19.358N 156.008W 0–1 EF989686

Hyperioides longipes Fort Pierce, FL, USA 27.348N 79.548W 0–100 EF989685

Hyperoche capucinus Weddell Sea 60.568S 52.818W 0–328 EF989665

Hyperoche martinezi California, USA 36.378N 122.108W 100–200 EF989668

Hyperoche medusarum California, USA 35.808N 122.858W 403 EF989667

Iulopis loveni Fort Pierce, FL, USA 27.348N 79.548W 0–100 EF989669

Jassa slatteryi UC Berkeley culture N/A N/A N/A EF989682

Lanceola loveni California, USA 36.378N 122.098W 1000 EF989693

Lanceola pacifica California, USA 35.508N 123.878W 1324 EF989697

Lanceola sayana California, USA 36.438N 124.078W 0–400 EF989696

Leptocotis tenuirostris Fort Pierce, FL, USA 27.348N 79.548W 0–100 EF989653

Lestrigonus schizogeneios Kona coast, HI, USA 19.358N 156.008W 0–1 EF989684

Lycaea nasuta Kona coast, HI, USA 19.428N 156.078W 0–1 EF989647

Lysianassoid California, USA 36.338N 122.908W 300–700 EF989712

Microphasma agassizi California, USA 36.438N 124.078W 0–400 EF989692

Mimonectes loveni California, USA 36.608N 122.388W 500–700 EF989698

Monoculodes sp. Fort Pierce, FL, USA 27.348N 79.548W 0–100 EF989705

Orchestia cavimana Tegeler See, GER 52.348N 13.158E 0 EF989708

Oxycephalus clausi Oahu, HI, USA 21.298N 158.238W BW EF989652

Paraoroides sp. Kewalo Basin Harbor 21.178N 157.518W 0–1 EF989711

Paraphronima gracilis California, USA 36.438N 124.078W 0–400 EF989674

Parapronoe cambelli Oahu, HI, USA 21.128N 158.198W 0–77 EF989657

Parhayle hawaiensis KML culture N/A N/A N/A EF989709

Phronima bucephala California, USA 36.438N 124.078W 0–400 EF989680

Phronima sedentaria California, USA 36.338N 122.908W 300–700 EF989679

Phronimella elongata ATL Fort Pierce, FL, USA 27.348N 79.548W 0–100 EF989677

(continued)


gene lineage relationships and bootstrap values weremapped to the most likely ML tree. Our combinedML COI analysis recovers three clades of hyperiidsnearly identical to those from our Bayesian results(Figs. 2, 3, and 4, Supplementary data). The mostlikely ML tree unites the three hyperiid clades.However, there is no bootstrap support for thisresult (Fig. 3, Supplementary data). With a highdegree of support, we also recovered monophyleticcaprellids (from the small number included in thisstudy) as branching from within the gammariids(Figs. 2 and 3, Supplementary data). An internalassessment of our results was by recapitulation of thetwo Lake Bailkal gammariid radiations (Macdonaldet al. 2005) and recapitulation of the Antarcticradiations of the Epimeria and Iphimediid gammar-iids (Lorz and Held 2004) (Supplementary data).

Although, we found many amphipod crown-grouprelationships to be highly supported, the majority ofthe deep nodal relationships among the Amphipodaare poorly supported and remain largely unresolvedfrom COI sequencing alone (Supplementary data).Interestingly, most hyperiid COI sequences havelong branches relative to the other amphipod

sequences examined. This is indicative of adifferential rate of change occurring among hyperiidCOI sequence clades relative to the other amphipodCOI sequences examined.

Morphological homoplasy among the Amphipodais a well-characterized phenomenon that has histori-cally confounded taxonomic descriptions (Barnardand Karaman 1991; Vinogradov et al. 1996), and theuse of molecular data for phylogenetic methodolo-gies is not immune from the effects of homoplasy. Atthe level of DNA sequences, homoplasy can manifestas site-specific variation that escapes detection due totwo proximate causes (1) inadequate taxon samplingwhich thereby misses phylogenetically informativesequence variation, and (2) a rapid rate of sequencechange among the taxa being examined whicheliminates evidence of past, phylogenetically useful,sequence variation. To assess the potential influenceof sequence homoplasy and to further characterizethe variation in branch lengths that we observedamong the taxa sampled, we generated a mutationsaturation plot. We used maximum parsimonyto generate a patristic distance matrix (Philippeand Forterre 1999). In a mutation saturation plot,

Table 1 Continued

Taxon Collection Locality Latitude Longitude Depth (m) COI Accession

Phronimella elongata PAC Oahu, HI, USA 21.268N 158.208W 0–680 EF989678

Phronimopsis spinifera Fort Pierce, FL, USA 27.348N 79.548W 0–100 EF989683

Phrosina semilunata ATL Fort Pierce, FL, USA 27.348N 79.548W 0–100 EF989670

Phrosina semilunata PAC Oahu, HI, USA 21.278N 158.148W 0–50 EF989671

Platyscelus serratulus Fort Pierce, FL, USA 27.348N 79.548W 0–100 EF989662

Primno brevidens California, USA 36.378N 122.108W 100–200 EF989672

Primno evansi Fort Pierce, FL, USA 27.348N 79.548W 0-100 EF989673

Rhabdosoma whitei Oahu, HI, USA 21.138N 158.168W 0–258 EF989650

Rhachotropis sp. California, USA 36.338N 122.908W 300–700 EF989704

Scina borealis California, USA 36.338N 122.908W 300–700 EF989699

Scypholanceola aestiva California, USA 36.438N 124.078W 0–400 EF989694

Scypholanceola sp. California, USA 35.488N 123.868W 1399 EF989695

Stenothoidae Waikiki, HI, USA 21.158N 157.508W 36 EF989710

Streetsia challengeri Oahu, HI, USA 21.278N 158.148W 0–50 EF989651

Synopia sp. Carrie Bowe Caye, BZ 16.478N 88.048W 0–10 EF989701

Themsito japonica Hokkaido, JN 42.008N 141.008E 0–500 EF989663

Themsito pacifica California, USA 36.438N 124.078W 0–400 EF989664

Thyropus sphaeroma Oahu, HI, USA 21.128N 158.198W 0–77 EF989661

Tryphana malmi California, USA 36.808N 121.808W 0–100 EF989656

Vibilia antartica Weddell Sea 60.948S 53.128W 0–353 EF989689

Vibilia propinqua California, USA 35.468N 122.508W BW EF989687

Vibilia viatrix California, USA 35.308N 123.528W BW EF989688

The BW abbreviation in the depth column indicates specimens collected by bluewater diving (depths between 1–30m).


Table 2 List of additional amphipod taxa and COI sequences from Genbank used in this study

Taxon COI Accession Taxon COI Accession

Abyssorchomene_sp U92669 Gammaracanthus_lacustris AY061796

Acanthogammarus_brevispinus AY926651 Gammarus_aequicaudus AY926667

Acanthogammarus_flavus AY061800 Gammarus_annulatus AY926668

Acanthogammarus_victorii AY926652 Gammarus_daiberi DQ300255

Amphithoe_longimana AY926653 Gammarus_duebeni AY926669

Armadillidium_vulgare AF255779 Gammarus_lacustris AY926671

Asellus_aquaticus AY531826 Gammarus_tigrinus DQ300242

Brandtia_lata AY926654 Gmelinoides_fasciata AY926675

Chaetogammarus_marinus AY926655 Gnathiphimedia_mandibularis AF451353

Chaetogammarus_obtusatus AY926656 Gnathiphimedia_sexdentata AF451354

Chydaekata_sp DQ838028 Hakonboekia_strauchii AY926676

Crangonyx_floridanus AJ968911 Hirondellea_dubia AY183359

Crangonyx_pseudogracilis AJ968903 Hyale_nilssoni AF520435

Crangonyx_serratus AY926658 Hyalella_azteca DQ464719

Cyamus_erraticus DQ095139 Hyalella_montezuma AY152807

Cyamus_gracilis DQ095105 Hyalella_muerta DQ464603

Cyamus_ovalis DQ095047 Hyalella_sandra DQ464682

Dikerogammarus_haemobaphes AY529049 Hyalella_simplex AF520434

Dikerogammarus_villosus AY529048 Iphimediella_cyclogena AF451348

Echiniphimedia_echinata AF451352 Iphimediella_georgei AF451349

Echiniphimedia_hodgsoni AF451350 Iphimediella_rigida AF451347

Echiniphimedia_waegelei AF451351 Maarrka_wollii DQ838034

Echinogammarus_ischnus AY326126 Macrohectopus_branickii AY926677

Echinogammarus_trichiatus AY529051 Megomaera_subtener AY926678

Eogammarus_confervicolus AY926659 Melita_nitida AY926679

Eogammarus_oclairi AY926660 Micruropus_crassipes AY926680

Epimeria_georgiana AF451341 Micruropus_fixseni AY926681

Epimeria_macrodonta AF451343 Micruropus_glaber AY926682

Epimeria_reoproi AF451342 Micruropus_wahli AY926683

Epimeria_robusta AF451344 Molina_pleobranchos DQ255962

Epimeria_rubrieques AF451345 Monoculodes_antarcticus AF451356

Epimeria_similis AF451346 Monoporeia_affinis AY926684

Eulimnogammarus_cruentus AY926661 Niphargus_fontanus DQ064702

Eulimnogammarus_cyaneus AY061801 Niphargus_rhenorhodanensis DQ064703

Eulimnogammarus_inconspicuous AY926662 Niphargus_virei DQ064749

Eulimnogammarus_maacki AY926663 Obesogammarus_crassus AY189482

Eulimnogammarus_viridulus AY926664 Odontogammarus_calcaratus AY926685

Eulimnogammarus_vittatus AY926666 Ommatogammarus_albinus AY926686

Eurythenes_gryllus U92660 Orchestia_uhleri AY152751

Eusirus_cf_perdentatus AF451355 Pallasea_cancellus AY926687

Eusirus_cuspidatus AY271852 Paramelitidae_sp DQ838036

Euxinia_maeoticus AY529038 Paramphithoe_hystrix AY271847

Exhyalella_natalensis AF520436 Perthia_sp DQ230097

Gammaracanthus_aestuariorum AY061798 Pilbarus_millsi DQ490125

Gammaracanthus_caspius AY061797 Poekilogammarus_pictoides AY926690

(continued)


the presence of a curve with a mutational plateauindicates that progressive saturation for mutationalchanges is occurring and thus there is a loss of thephylogenetic signal necessary for accurately resolvingdeep branching nodes (Philippe et al. 1994; Philippeand Forterre 1999).

Our scatter plot of observed versus inferred COIsubstitutions has an atypical, wide, cloud-likedistribution (Fig. 5A). In general, there were fewerobserved substitutions than predicted to haveoccurred between COI sequence pairs. No plateaucorresponding to COI mutational saturation couldbe easily discerned from the full data set. Samplingsubsets of COI sequence, however, revealedthree distinguishable patterns of COI gene variationsegregating among the taxa in this study (Fig. 5B–D).This indicates divergent, nonuniform, patterns ofsequence change among COI gene lineages in theAmphipoda.

Pair-wise comparisons among the three hyperiidclades demonstrates that among these taxa there is asaturation curve containing many observed substitu-tions that are relatively close to inferred substitutionsas well as an expected mutational plateau (Fig. 5B).Therefore, although the hyperiid COI branches aregenerally longer than the other amphipod sequencesconsidered, they should contain sufficient sequencevariation to reliably resolve many crown-grouprelationships (Fig. 4). Each of the three detectedhyperiid COI clades independently retains the generalshape of this curve (Supplementary data).

Superimposing pair-wise comparisons between thelargest recovered monophyletic gammariid COI cladeexclusive of hyperiid sequences (Fig. 2) reveals acloud-like cluster (Fig. 5C). The cluster of substitu-tion values does not display a discernable curve andplateau trend. The cluster departs strongly from theideal observed/inferred substitution ratio, and asignificant proportion of pair-wise values exhibitlow inferred substitution values coupled with lowobserved substitution values. This supports thegeneral observation of shorter branch lengthsobserved in this gammariid clade. The shape ofthis cluster strongly suggests that mutational satura-tion has removed most of the phylogenetic

signal associated with comparisons between thesesequences. Indeed, a majority of the nodes in thisclade are characterized by low Bayesian posteriorprobabilities and no ML bootstrap support, and thedeep nodes in particular are not well supported(Fig. 2).

Finally, superimposing pair-wise comparisonsbetween the hyperiids and all other amphipod taxaresults in an additional informative shift inthe cluster of substitution values (Fig. 5D).The distribution of the values observed in thiscase suggests that the majority of the pair-wisecomparisons between gammarid and hyperiid COIsequences have particularly low phylogenetic signal,as observations of sequence substitution fall drama-tically relative to inferred sequence substitutions.Consideration of the shape of clustered values inFig. 5C and D confirms that mutational saturationfor COI has occurred among the gammarid amphi-pods included in this analysis. The observation ofhomoplasy among gammarid versus gammariid andgammariid versus hyperiid COI sequences does notprevent reconstruction of lineage relationships withinhyperiid clades. However, COI sequence homoplasydoes prevent the accurate recovery of relationshipsbetween the three recovered hyperiid clades thatcontain deeper nodes that may interdigitate withill-defined gammariid taxa.

Discussion

The phylogeny of pelagic midwater hyperiidamphipods

The histories of patterns of descent by modificationare difficult to discern when shared attributes arethe result of convergence. Among the Amphipoda,morphological convergence (homoplasy) is welldocumented. To help improve our understandingof uncertain relationships and the relative impor-tance of morphological characters, we examined theCOI gene among 168 amphipodan taxa including52 hyperiids. Our results indicate that there mayhave been as many as three independent radiationsamong the hyperiids. In addition, our COI datasuggest taxonomic affinities for several previously

Table 2 Continued

Taxon COI Accession Taxon COI Accession

Pontogammarus_abbreviatus AY926691 Rhachotropis_inflata AY271854

Pontogammarus_obesus AY529041 Synurella_sp AJ968914

Pontogammarus_robustoides AY529047 Uroctena_sp DQ230128

Rhachotropis_aculeata AY271853 Ventiella_sulfuris U92667


enigmatic hyperiid taxa. Bayesian results suggest thatat least one of the hyperiid radiations (hyperiid clade1 in Fig. 2) may be an early diverging lineage withinAmphipoda. Our Bayesian results also suggest thatthe hyperiids are likely to be polyphyletic (Fig. 2).

ML results unite the three hyperiid clades but withno bootstrap support (Fig. 3). We also find a highlysupported monophyletic clade of caprellids from theCOI sequence data included in this analysis. In ouranalyses, the caprellid clade is always sister to the

Fig. 2 COI Bayesian analysis combined consensus tree. Consensus tree is the post burn-in tree from four combined independent runs.

Branch nodes with Bayesian posterior probability support greater than 95% are marked with black circles. Black triangles represent

collapsed views of the three recovered hyperiid clades. Grey triangle represents collapsed view of the caprellid clade. Bayesian

consensus tree topology proposes a sister group relationship between hyperiid clade 2 and hyperiid clade 3 but with low confidence.

A majority of the lineage relationships between taxa within the hyperiid clades have high support values (Fig. 4). In contrast, the vast

majority of deep branching node hypotheses are unsupported by COI sequence data.


lineage that includes the ischyrocerid J. slatteryi(Supplementary data). This result is in agreementwith recent morphological analyses of corophiid andcaprellid groups (Myers and Lowry 2003). COIsequence variation among the amphipod taxa

sampled does not, however, resolve either therelationships between separate hyperiid radiationevents or the relationships of lineages among themajority of the gammarids due to inadequateresolution at deeper nodes.

Fig. 3 COI Maximum likelihood tree. ML tree is the most likely tree from four independent runs. Branch nodes with bootstrap support

greater than 95% are marked with black circles. Black triangles represent collapsed views of the three recovered hyperiid clades.

Grey triangle represents collapsed view of the caprellid clade. The most likely ML tree topology proposes a sister group relationship

among all three hyperiid clades. This relationship has no bootstrap support. Many lineage relationships between taxa within the

hyperiid clades have high support values (Fig. 4). In contrast, the vast majority of deep branching nodes have no bootstrap support

(Supplementary data).


Several interesting observations from our preli-minary molecular analysis of the hyperiids can bemade. First, there is a fair amount of agreementbetween the clades recovered in our molecular results(Fig. 4) and traditional taxonomic groupings ofhyperiids based on morphology alone (Vinogradovet al. 1996). For example, several monophyleticlineages composed of classical taxonomic groupingsare recovered in our analyses including theinfraorder Physosomata within clade 2, and thesuperfamilies Platysceloidea, Vibilioidea, andPhronimoidea within clade 1 and clade 3, respec-tively (Fig. 4, Supplementary data).

However, a number of interesting questionsregarding hyperiid relationships arise from our

analyses. For example, traditional morphologicalexaminations have been unable to confidently placethe genus Cystisoma relative to other hyperiidtaxa (Vinogradov et al. 1996; Zeidler 2003a). Inour analyses, Cystisoma appears to diverge at thebase of clade 2 (Fig. 4, Supplementary data) thatincludes representatives of the classically definedinfraorder Physosomata (Vinogradov et al. 1996).Additional sampling of Cystisoma and othermembers of clade 2 are needed to further explorethis inferred relationship. Among the representativesof clade 1, we consistently recovered, albeit withlow support, Lycaea nasuta splitting the classicallydefined family Oxycephalidae (Fig. 4, Supplementarydata) suggesting that Oxycephalidae, as currently

Fig. 4 Inferred hyperiid relationships from COI analyses. The three hyperiid clades are represented here from the Bayesian concensus

tree shown in Fig. 2. Branch nodes show Bayesian posterior probability support above and ML bootstrap support value below. The

clade topologies represented here are consistently recovered between independent Bayesian and ML runs (Supplementary data).


Fig. 5 Mutation saturation scatter plots. The Y-axis is the observed number of differences between pairs of COI sequences. The X-axis

is the inferred number of differences between pairs of COI sequences determined using maximum parsimony methods. Each circle

represents an observed versus inferred substitution value for a pair of COI sequences. The black line represents the ideal unsaturated

case in which the number of observed substitutions equals the number of inferred substitutions. Diagrams on the right indicate which

groups of taxa (black circles) are being compared in each panel. (A) Among Amphipoda sampled, observed versus inferred COI

substitutions have a wide cloud-like distribution. In general, there are fewer observed substitutions than predicted to have occurred

between COI sequence pairs. No plateau corresponding to COI mutational saturation can be easily discerned from the full dataset.

(B) The black circles indicate pair-wise comparisons between hyperiid COI sequences. Each of the three detected hyperiid COI clades

can be superimposed on this curve (Supplementary data). The distribution of hyperiid values is a well-defined subset showing a distinct

plateau that indicates mutational saturation among the hyperiid COI sequences as the number of predicted substitutions increases in the

absence of observed substitutions among the pair-wise comparisons. Additionally, the curve corresponds with the general observation

of longer branch lengths associated with members of the three hyperiid COI clades relative to gammariid COI clades. (C) The black

circles indicate pair-wise comparisons between the largest monophyletic gammariid COI clade exclusive of hyperiid sequences. The

distribution of gammariid values reflect shorter branch lengths among gammariid COI sequences. The shape of the cloud-like

cluster suggests that these sequences have low relative phylogenetic signal relative to COI sequence comparisons between hyperiids.

(D) The black circles indicate pair-wise comparisons between gammariid and hyperiid COI sequences. The distribution of the values

observed in this case suggest that the majority of the pair-wise comparisons between gammarid and hyperiid COI sequences have

low phylogenetic signal as observations of sequence substitution fall dramatically relative to inferred sequence substitutions.


recognized (Vinogradov et al. 1996), maybe poly-phyletic. Further sampling between Lycaea andother members of the Oxycephalidae would beinformative with regard to this tentative result.We also consistently recovered Tryphana malmi asa well-supported member of clade 3, whereasmorphological analysis alone suggests Tryphanawould be affiliated with the Platysceloidea (andthus clade 1 in our analyses). This is a rathersurprising result that suggests further analyses ofTryphana relative to members of both clade 1 andclade 3 are warranted.

The presence of significant intraspecific variationin COI has been used among some amphipod groupsto discriminate between populations of closelyrelated species (Meyran et al. 1997; Witt et al.2003; Kaliszewska et al. 2005; Lefebure et al. 2006;Witt et al. 2006). In our analysis we sampled twomonotypic genera, Phronimella elongata and Phrosinasemilunata, from both the Central Pacific and theAtlantic Gulf Stream. Both are members of hyperiidclade 3 (Fig. 4). We recovered surprisingly longbranch-lengths between Pacific and Atlantic isolates.Two alternative scenarios can be considered.The COI sequence divergence could indicatecryptic speciation within these two genera that havehistorically been considered monotypic. Alternatively,it could represent substantial isolation and diver-gence of the panoceanic populations of these twospecies. Further comparisons between populations ofthese taxa from both the Atlantic and the Pacificoceans, are warranted.

One of the main mechanisms contributing tosequence homoplasy and the loss of phylogeneticsignal is site-specific mutational saturation (Philippeet al. 1994; Philippe and Forterre 1999). Our testfor mutational saturation among the COI sequencesused in this analysis indicates saturation (lossof phylogenetic signal) among the majority ofgammarid COI sequences (Fig. 5C). Comparisonsbetween hyperiid COI sequences demonstrate differ-ential evolution of this gene and the retention ofphylogeneticaly significant information among thesesequences (Fig. 5B, Supplementary data). However,the low signal present among the majority of thegammarid sequences included prevent the recoveryof lineage relationships outside of the three well-supported hyperiid clades.

Morphological and molecular homoplasy play acentral role in evolutionary biology and representmajor impediments to understanding links betweenorganismal genotype and phenotype. Improvingsupport for deep branching nodes withinAmphipoda is crucial to hypothesizing credible

evolutionary relationships of the hyperiid radiationsreported here to other amphipodan faunas. Futureanalyses should include multiple genetic loci fromboth mitochondrial and nuclear markers to moderatethe effects of differential rates of gene evolution.Increased taxon sampling is also urgently needed tobetter represent the enormous diversity of extantAmphipoda (currently more than 8000 describedspecies). Hypotheses generated from these additionalmolecular analyses can, and should be, used toindependently evaluate morphological attributes thatappear to play important roles in patterns ofamphipod diversity but that have proven recalcitrantto traditional morphological based evolutionaryanalyses due to homoplasy. Given the high branchsupport observed within hyperiid clades in ouranalysis, independent contrast methodologies couldprove particularly useful in exploring morphologicalcharacter convergence within and between theselineages (Felsenstein 1985).

For a number of reasons, the expansion ofsampled genetic loci and the inclusion of additionaltaxa should be undertaken to further improve lineagerelationships within the hyperiid clades identifiedhere. Pelagic hyperiid amphipods have very sharpdifferences in the organization of their heads andanterior nervous systems relative to most otherbenthic amphipods, likely due to constraintsimposed by disparate life histories (W.E.B., personalobservation). Clearly, associations of hyperiids withgelatinous zooplankton are sufficiently old tohave played an important role in the evolution ofvarious hyperiid morphologies, as evidenced by themodifications of appendages used for feedingon/with and for attachment to their preferred hosts(Bowman and Gruner 1973; Vinogradov et al. 1996).Many ecdysozoans (e.g., crustaceans, insects, cheli-cerates, nematodes, and nematomorphs) haverepresentatives that possess a parasitic life history(Price 1977; Poulin and Morand 2000). Coevolutionbetween hosts and their parasites is well character-ized as leading both to strong stabilizing and strongdestabilizing selection (Frank 1993). As detailsof associations between hyperiids and gelatinouszooplankton continue to emerge, it will be importantto consider the role that hosts have played during theevolution of various hyperiid lineages. For example,in contrast to the majority of benthic amphipods, thehyperiids exhibit a range of posthatching larval stagesthat in most cases reflect specific interactions withpreferred hosts (Laval 1980). We suggest that thehyperiid amphipods offer a unique intersection ofattributes that further our understanding of biologi-cal evolution; they are members of an extremely


successful clade of metazoans, display a range ofparasitic associations, and are well adapted to thelargest habitat on the planet.

Supplementary data

Supplementary data are available at ICB online.

Acknowledgments

This work has been supported by the NSF (W.E.B.,DBI-0310269; M.Q.M., EF-0334871) and the NAS(W.E.B.). This work has also benefited substantiallyfrom access to Smithsonian Institution field stations:the Smithsonian Institution Caribbean Coral ReefEcosystems (CCRE) Program at Carrie Bowe Cayeas contribution #806 (partially supported by theHunterdon Oceanographic Research Fund), theSmithsonian Tropical Research Institution (STRI) atBocas del Toro (partially supported by the HunterdonOceanographic Research Fund), and the SmithsonianMarine Station at Fort Pierce. We thank the UHDiving Safety Program for providing OC and CCRSCUBA training and support. Specimens critical tothis study were contributed by Robert L. Humphreys,Karen Osborn, Nipam H. Patel, Rebecca ScheinbergHoover, Carsten Wolff, Wolfgang Zeidler, and thepilots of MBARI’s ROVs, Tiburon and Ventana.We thank Casey W. Dunn for computation advice.We also thank the following for discussion andproviding critical comments that have significantlyimproved this communication: Rebeca Gasca, Wolf-gang Zeidler, Casey W. Dunn, Andreas Hejnol, DavidQ. Matus, and Amy Maxmen.

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Phronimella_elongata_ATL

Lanceola_pacifica

Poekilogammarus_pictoides

Eulimnogammarus_cruentus

Gammarid_Tib750

Calamorhynchus_pellucidus

Thyropus_sphaeroma

Ventiella_sulfuris

Pilbarus_millsi

Paramphithoe_hystrix

Cystisoma_gershwinae

Brachyscelus_globiceps

Lanceola_loveni

Echinogammarus_ischnus

Synurella_sp

Vibilia_antartica

Platyscelus_serratulus

Dikerogammarus_haemobaphes

Armadillidium_vulgare

Hirondellea_dubia

Acanthogammarus_victorii

Orchestia_uhleri

Cranocephalus_scleroticus

Gammarus_duebeni

Eulimnogammarus_cyaneus

Eusirus_cuspidatus

Macrohectopus_branickii

Epimeria_reoproi

Hyperoche_capucinus

Hyalella_muerta

Themisto_pacifica

Cystisoma_pellucida

Brachyscelus_rapax

Glossocephalus_sp

Gmelinoides_fasciata

Crangonyx_pseudogracilis

Epimeria_rubrieques

Paraoroides_sp

Cilicaea_sp

Crangonyx_serratus

Jassa_slatteryi

Hyalella_azteca

Gammarus_annulatus

Phronimopsis_spiniferaLestrigonus_schizogeneios

Lanceola_sayana

Microphasma_agassizi

Micruropus_wahli

Themisto_japonica

Gammarid_Tib844

Lysianassoid_AP036

Molina_pleobranchos

Hyperioides_longipes

Echinogammarus_trichiatusObesogammarus_crassus

Iphimediella_georgei

Pontogammarus_abbreviatus

Eulimnogammarus_viridis

Iulopis_loveni

Gammaracanthus_aestuariorum

Vibilia_viatrix

Mimonectes_loveni

Hakonboekia_strauchii

Cyamus_erraticus

Hyperia_macrocephala

Hyalella_montezuma

Epimeria_similis

Pallasea_grubei

Gammarus_oceanicus

Niphargus_rhenorhodanensis

Dikerogammarus_villosus

Chaetogammarus_obtusatusChaetogammarus_marinus

Tryphana_malmi

Gammarid_KML

Acanthogammarus_flavus

Niphargus_virei

Hyalella_sandra

Stenothoidae

Eulimnogammarus_maacki

Primno_evansi

Rhachotropis_aculeata

Scypholanceola_sp

Gammarus_daiberi

Parhyale_hawaiensis

Hyalella_simplex

Rhachotropis_inflata

Rhachotropis_sp

Iphimediella_cyclogena

Gammarus_tigrinus

Brandtia_lata

Oxycephalus_clausi

Cyamus_gracilis

Echiniphimedia_waegelei

Monoporeia_affinis

Glossocephalus_milneedwardsi

Phrosina_semilunata_PAC

Paraphronima_gracilis

Synopia_sp

Gnathiphimedia_mandibularis

Euxinia_maeoticus

Asellus_aquaticus

Cyphocaris_sp

Scypholanceola_aestiva

Gnathiphimedia_sexdentata

Eogammarus_confervicolus

Gammarus_lacustris

Rhabdosoma_whitei

Eurythenes_gryllus

Hyperoche_medusarum

Epimeria_georgiana

Micruropus_glaber

Eusirus_cf_perdentatus

Phronima_bucephala

Vibilia_propinqua

Hyperoche_martinezi

Abyssorchomene_sp

Plesiogammarus_brevis

Cyllopus_magellanicus

Hyale_nilssoni

Cyamus_ovalis

Amphithoe_longimana

Gammaracanthus_lacustris

Uroctena_sp

Hyperietta_parviceps

Phronima_sedentaria

Acanthogammarus_brevispinus

Phrosina_semilunata_ATL

Monoculodes_sp

Echiniphimedia_echinata

Megomaera_subtener

Scina_borealis

Ommatogammarus_albinus

Gammarus_aequicaudus

Eulimnogammarus_vittatus

Acanthoscina_acanthodes

Capprellid_KBH

Gammaracanthus_caspius

Pontogammarus_obesus

Echiniphimedia_hodgsoni

Primno_brevidens

Odontogammarus_calcaratus

Exhyalella_natalensis

Leptocotis_tenuirostris

Maarrka_wollii

Orchestia_cavimana

Parapronoe_cambelli

Epimeria_robusta

Pallasea_cancellus

Lycaea_nasuta

Crangonyx_floridanus

Brachyscelus_crusculum

Micruropus_fixseni

Eulimnogammarus_inconspicuous

Streetsia_challengeri

Chydaekata_sp

Iphimediella_rigida

Paramelitidae_sp

Phronimella_elongata_PAC

Melita_nitida

Micruropus_crassipes

Cyllopus_lucasii

Epimeria_macrodonta

Monoculodes_antarcticus

Perthia_sp

Pontogammarus_robustoides

Niphargus_fontanus

Eogammarus_oclairi

0.26

0.99

1

0.53

1

1

0.83

0.3

1

0.07

0.3

1

0.98

0.39

0.98

1

1

0.82

0.64

0.05

0.1

1

1

0.99

1

0.23

0.97

1

1

0.48

0.57

1

1

0.74

1

0.99

1

0.63

1

1

0.46

1

0.54

1

1

0.98

0.66

0.85

1

0.29

0.95

0.98

1

1

0.22

0.26

0.63

0.81

0.96

0.94

0.69

1

1

0.98

0.83

1

0.16

0.34

1

1

0.19

0.97

0.33

0.89

0.51

0.33

0.27

0.62

0.98

1

1

1

1

1

0.97

1

0.34

0.29

0.59

0.99

1

0.99

0.93

0.98

0.93

0.84

1

0.75

0.45

1

0.22

0.68

0.92

0.91

0.35

0.56

0.95

1

0.61

0.1

0.98

0.17

0.65

1

0.48

0.67

0.52

1

1

1

0.49

1

1

1

0.39

1

1

0.96

0.97

0.65

0.74

0.7

0.54

0.95

0.51

1

0.96

0.63

0.95

0.12

0.59

0.7

0.72

1

1

0.93

1

0.05

0.45

1

1

0.56

0.87

0.66

0.89

1

0.92

1

1

0.53

1

0.72

1

0.62

0.98

0.2

hyperiidclade 3

hyperiidclade 2

caprellid

hyperiidclade 1


Amphithoe_longimana


Niphargus_virei



Micruropus_fixseni

Hyperoche_martinezi

Capprellid_KBH

Stenothoidae


Epimeria_rubrieques






Pilbarus_millsi


Cyamus_gracilis


Thyropus_sphaeroma

Lanceola_sayana

Perthia_sp


Gammarus_oceanicus

Vibilia_viatrix



Ventiella_sulfuris





Epimeria_robusta


Asellus_aquaticus

Monoculodes_sp

Parapronoe_cambelli


Mimonectes_loveni



Scypholanceola_sp

Lanceola_loveni

Hyalella_azteca



Iphimediella_rigida

Hirondellea_dubia

Gammarus_daiberi

Lysianassoid

Cilicaea_sp


Themisto_japonicaThemisto_pacifica

Cyllopus_lucasii



Cyphocaris_sp


Chaetogammarus_marinus


Synurella_sp

Melita_nitidaMegomaera_subtener

Cystisoma_pellucida

Lycaea_nasuta

Gammarid_Tib750

Uroctena_sp

Pallasea_grubei

Phronimopsis_spinifera

Hyalella_montezuma

Scina_borealis

Primno_brevidens

Gammarus_annulatus

Vibilia_propinquaTryphana_malmi

Eogammarus_oclairi

Orchestia_cavimana


Jassa_slatteryi

Vibilia_antartica

Abyssorchomene_sp


Monoporeia_affinis

Obesogammarus_crassus


Brandtia_lata

Micruropus_glaber

Epimeria_reoproi



Chydaekata_sp

Molina_pleobranchos

Gammarid_KML

Synopia_sp




Pallasea_cancellus

Gammarus_lacustris


Maarrka_wollii

Brachyscelus_rapax

Micruropus_wahli

Gammarus_tigrinus

Hyalella_muerta

Rhabdosoma_whitei

Orchestia_uhleri


Phronima_bucephala



Hyalella_simplex

Hyperoche_capucinus

Epimeria_similis

Paramelitidae_sp

Eurythenes_gryllus




Niphargus_fontanus


Epimeria_georgiana

Rhachotropis_sp



Lestrigonus_schizogeneios

Euxinia_maeoticus

Phronima_sedentaria

Cyamus_ovalis

Echinogammarus_trichiatus


Parhyale_hawaiensis



Crangonyx_serratus

Oxycephalus_clausi

Epimeria_macrodonta

Hyalella_sandra





Gammarid_Tib844

Paraoroides_sp



Primno_evansi


Gammarus_duebeni


Iphimediella_georgeiIphimediella_cyclogena

Hyperoche_medusarum

Cyamus_erraticus

Glossocephalus_sp


Eusirus_cuspidatus





Chaetogammarus_obtusatus

Iulopis_loveni

Hyale_nilssoni

Lanceola_pacifica

0.82

0.48

0.98

0.91

1

0.99

0.94

0.43

1

0.96

0.63

0.45

0.21

1

0.47

0.95

0.62

0.4

0.73

0.12

1

0.26

1

0.56

1

0.64

1

0.691

0.68

0.6

1

0.06

0.81

0.41

0.91

1

0.62

0.31

0.59

0.62

1

1

1

0.95

0.5

0.44

1

0.99

0.6

0.98

0.98

0.87

1

0.48

0.94

1

0.79

0.95

0.95

0.25

0.51

0.64

0.39

0.24

0.82

0.82

1

0.94

0.94

1

0.51

1

0.95

1

0.27

1

1

0.38

0.55

0.32

0.96

1

1

0.27

1

0.61

0.52

0.96

1

1

1

0.99

1

0.53

0.47

0.68

0.38

0.71

1

0.52

0.14

0.57

0.97

1

0.17

0.63

0.94

0.94

1

1

0.99

1

0.97

0.24

1

0.16

1

0.95

1

0.44

0.91

0.86

0.9

1

0.77

1

1

0.33

0.91

0.86

1

1

0.96

0.56

0.93

0.93

0.81

1

1

0.98

0.57

0.64

0.18

0.93

1

0.64

0.93

1

1

0.33

0.14

0.9

0.45

0.99

1

0.71

0.93

1

0.17

1

1

0.98

0.87

1

0.2

hyperiidclade 3

hyperiidclade 2

hyperiidclade 1

caprellid

Armadillidium vulgare

Melita nitidaMegomaera subtener

100

Lycaea nasutaCranocephalus scleroticus

Calamorhynchus pellucidusStreetsia challengeri

9471

Oxycephalus clausi

60

Rhabdosoma whiteiLeptocotis tenuirostris

9996

60

Glossocephalus milneedwardsiGlossocephalus sp

100

75

Brachyscelus crusculumBrachyscelus rapax

100

Brachyscelus globiceps

100

100

Parapronoe cambelli

100

Thyropus sphaeromaPlatyscelus serratulus

100

100

95

Tryphana malmi Themisto japonica

Themisto pacifica 100

Hyperoche capucinus Hyperia macrocephala

Hyperoche medusarum 97

61

Hyperoche martinezi Iulopis loveni

4784

100

Phronimopsis spinifera Lestrigonus schizogeneios 1.00

Hyperioides longipes Hyperietta parviceps

100100

54

Phronimella elongata ATL Phronimella elongata PAC

100

Phronima bucephala 99

Phronima sedentaria 100

63

Phrosina semilunata ATL Phrosina semilunata PAC

100

Primno brevidens Primno evansi

10099

93

100

Vibilia propinqua Vibilia viatrix

100

Vibilia antartica 100

Cyllopus magellanicus Cyllopus lucasii

100100

93

Paraphronima gracilis

100

Synopia sp

83

Lysianassoid Abyssorchomene sp

100

57

Perthia spSynurella sp

78

47

Gammarid Tib844Paraoroides sp

Hyalella sandra100

35

Hyalella aztecaHyalella muerta

59

Hyalella montezuma100

55

Hyalella simplex

37

55

Capprellid KBHCyamus erraticus

Cyamus gracilisCyamus ovalis

100100

100

Jassa slatteryi

100

Amphithoe longimana

96

Stenothoidae

100

42

Exhyalella natalensisHyale nilssoni

50

Eogammarus confervicolusEogammarus oclairi

10057

77

Parhyale hawaiensis

60

Orchestia cavimana Orchestia uhleri

69

65

Pontogammarus abbreviatusPontogammarus obesus

100

Euxinia maeoticusPontogammarus robustoides

9695

Dikerogammarus haemobaphesDikerogammarus villosus

9588

Obesogammarus crassus

94

Echinogammarus trichiatusEchinogammarus ischnus

97100

36

Gammarid KMLEurythenes gryllus

94

Gammaracanthus aestuariorumGammaracanthus caspius

100

Gammaracanthus lacustris100

85

Chaetogammarus obtusatusChaetogammarus marinus

100

Uroctena spChydaekata sp

Pilbarus millsi50

Paramelitidae spMaarrka wollii

10082

Molina pleobranchos

99

61

Monoporeia affinis

29

45

57

Monoculodes sp Epimeria rubrieques

Epimeria georgiana85

Epimeria robusta100

Epimeria reoproiEpimeria macrodonta

63

Epimeria similis100

100

69

Eusirus cf perdentatusEusirus cuspidatus

90

Paramphithoe hystrix60

Monoculodes antarcticus

45

30

Hirondellea dubiaVentiella sulfuris

100

11

7

Hakonboekia strauchiiPoekilogammarus pictoides

100

Brandtia lataAcanthogammarus flavus

50

Eulimnogammarus viridisEulimnogammarus vittatus

Ommatogammarus albinus47

Eulimnogammarus maacki27

28

Eulimnogammarus cruentus

63

Plesiogammarus brevisEulimnogammarus inconspicuous

50

Eulimnogammarus cyaneus62

69

59

Pallasea cancellusOdontogammarus calcaratus

46

Pallasea grubeiAcanthogammarus victorii

9933

66

Acanthogammarus brevispinus

98

100

Micruropus glaberMicruropus crassipes

100

Micruropus wahli99

Gmelinoides fasciata

100

97

Gammarus duebeniGammarus aequicaudusGammarus lacustris

46

Micruropus fixseniMacrohectopus branickii

9546

56

Gammarus oceanicus

91

61

Gammarus annulatusGammarus daiberi

Gammarus tigrinus100

100

84

10

5

Cystisoma gershwinae Cystisoma pellucida

100

Microphasma agassizi Lanceola loveni

Scypholanceola sp

100

Lanceola sayana 52 Scypholanceola aestiva 100

Lanceola pacifica

65

100

Scina borealis

100

Mimonectes loveni

87

Acanthoscina acanthodes

100

69

Iphimediella rigidaIphimediella georgei

100

Echiniphimedia echinataEchiniphimedia waegelei

Echiniphimedia hodgsoni96

97100

Iphimediella cyclogena

98

Gnathiphimedia sexdentata

100

Gnathiphimedia mandibularis

100

20

1

Rhachotropis sp.Rhachotropis inflata

Rhachotropis aculeata50

99

Gammarid Tib750Niphargus fontanus

Niphargus rhenorhodanensisNiphargus virei

3710078

63

13

Cyphocaris spCrangonyx floridanus

Crangonyx pseudogracilis100

36

Crangonyx serratus25

30

100

Asellus aquaticusCilicaea sp

48

.1

hyperiidclade 3

hyperiidclade 2

caprelliid

hyperiidclade 1

outgroups

Armadillidium vulgare

Melita nitidaMegomaera subtener

99

Lycaea nasutaCranocephalus scleroticus

Calamorhynchus pellucidusStreetsia challengeri

9270

Oxycephalus clausi61

Rhabdosoma whiteiLeptocotis tenuirostris

10096

60

Glossocephalus milneedwardsiGlossocephalus sp.

100

73

Brachyscelu s crusculumBrachyscelu s rapax

100

Brachyscelus globiceps100

100

Parapronoe cambelli

100

Thyropus sphaeromaPlatyscelu s serratulus

100

100

97

Tryphana malmiThemisto japonica

Themisto pacifica100

Hyperoche capucinusHyperia macrocephala

Hyperoche medusarum97

57

Hyperoche martinezi

50

Iulopis loveni82

100

Phronimopsi s spiniferaLestrigonus schizogeneios

100

Hyperioides longipesHyperietta parviceps

100100

64

Phronimella elongata ATLPhronimella elongata PAC

100

Phronima bucephala98

Phronima sedentaria100

71

Phrosina semilunata ATLPhrosina semilunata PAC

100

Primno brevidensPrimno evansi

10099

93

99

Vibilia propinquaVibili a viatrix

100

Vibilia antartica100

Cyllopus magellanicusCyllopus lucasii

100100

94

Paraphronim a gracilis

99

Cystisoma gershwinaeCystisoma pellucida

100

Microphasma agassiziLanceola loveniScypholanceola sp.

100

Lanceola sayana54

Scypholanceola aestiva100

Lanceola pacifica

62

100

Scina borealis

100

Mimonectes loveni

58

Acanthoscina acanthodes

100

100

42

Capprellid KBHCyamus erraticus

Cyamus gracilisCyamus ovalis

100100

100

Jassa slatteryi

100

Amphithoe longimana

96

Stenothoidae

100

35

Synopia spLysianassoi d

Abyssorchomene sp100

47

Perthia spSynurell a sp

5814

Gammarid Tib844Paraoroides sp

Hyalell a sandra100

48

Hyalella aztecaHyalell a muerta

59

Hyalella montezuma100

51

Hyalell a simplex

27

12

10

Exhyalell a natalensisHyale nilssoni

66

Eogammarus confervicolusEogammaru s oclairi

10041

26

Parhyale hawaiensis

16

Orchestia cavimanaOrchesti a uhleri

74

22

Cyphocaris spCrangonyx floridanus

Crangonyx pseudogracilis100

43

Crangony x serratus

46

Gammarid T4Rhachotropi s inflata

Rhachotropis aculeata54

100

Gammarid Tib750Niphargus fontanus

Niphargus rhenorhodanensis39

Niphargu s virei97

71

45

9

Gammarid KMLEurythene s gryllus

94

Gammaracanthu s aestuariorumGammaracanthus caspius

100

Gammaracanthu s lacustris100

86

Chaetogammarus obtusatusChaetogammarus marinus

100

Uroctena spChydaekata sp

Pilbaru s millsi53

Paramelitida e spMaarrk a wollii

10082

Molina pleobranchos

99

93

Monoporei a affinis

44

66

82

Hakonboekia strauchiiPoekilogammarus pictoides

100

Brandtia lataAcanthogammarus flavus

52

Eulimnogammaru s viridisEulimnogammaru s vittatus

Ommatogammarus albinus46

Eulimnogammarus maacki27

27

Eulimnogammarus cruentus

65

Plesiogammaru s brevisEulimnogammarus inconspicuous

51

Eulimnogammarus cyaneus63

65

59

Pallasea cancellusOdontogammarus calcaratus

47

Pallasea grubeiAcanthogammaru s victorii

9933

66

Acanthogammaru s brevispinus

98

100

Micruropu s glaberMicruropu s crassipes

100

Micruropu s wahli100

Gmelinoides fasciata100

98

Gammarus duebeniGammarus aequicaudus

Gammarus lacustris47

Micruropu s fixseniMacrohectopu s branickii

9446

60

Gammarus oceanicus

92

60

Gammarus annulatusGammarus daiberi

Gammarus tigrinus100

100

82

10

Monoculodes spEpimeri a rubrieques

Epimeria georgiana86

Epimeria robusta100

Epimeri a reoproiEpimeria macrodonta

64

Epimeri a similis100

100

78

Eusirus cf perdentatusEusirus cuspidatus

91

Paramphitho e hystrix55

Monoculodes antarcticus

32

31

Hirondellea dubiaVentiell a sulfuris

96

11

16

Iphimediell a rigidaIphimediell a georgei

100

Echiniphimedia echinataEchiniphimedi a waegelei

Echiniphimedia hodgsoni96

97100

Iphimediell a cyclogena

98

Gnathiphimedia sexdentata

100

Gnathiphimedi a mandibularis

100

18

16

Pontogammarus abbriviatusPontogammarus obesus

100

Euxinia maeoticusPontogammarus robustoides

9593

Dikerogammarus haemobaphesDikerogammaru s villosus

9489

Obesogammarus crassus

93

Echinogammaru s trichiatusEchinogammarus ischnus

97

100

37

29

100

Asellus aquaticusCilicaea sp

57

.1

hyperiidclade 1

hyperiidclade 2

hyperiidclade 3

outgroups

caprelliid



Phronimopsis_spinifera

Hyperoche_medusarum




Tryphana_malmi


Cyphocaris_sp

Primno_brevidens

Gammarid_Tib750

Niphargus_fontanus

Cyamus_ovalis


Hyalella_montezuma


Epimeria_reoproi

Parhyale_hawaiensis

Themisto_japonica

Niphargus_virei


Vibilia_viatrix





Rhabdosoma_whitei

Iphimediella_rigida

Stenothoidae




Thyropus_sphaeroma


Echinogammarus_trichiatus

Vibilia_antartica



Epimeria_similis

Hyperoche_martinezi


Uroctena_sp

Cystisoma_pellucida

Mimonectes_loveni


Obesogammarus_crassus


Hirondellea_dubia

Cyllopus_lucasii

Cyamus_gracilis

Primno_evansi

Lycaea_nasuta



Brachyscelus_rapax


Paramelitidae_sp


Hyalella_azteca


Epimeria_georgiana


Gammarid_Tib844


Molina_pleobranchos

Perthia_sp

Hyalella_muerta


Jassa_slatteryi


Cilicaea_sp

Phronima_bucephala

Parapronoe_cambelli

Scina_borealis

Chydaekata_sp


Ventiella_sulfuris

Euxinia_maeoticus



Iulopis_loveni

Gammarus_lacustris

Megomaera_subtener

Pallasea_cancellus

Abyssorchomene_sp


Gammarus_tigrinus



Gammarus_duebeni

Monoculodes_sp


Lestrigonus_schizogeneios

Micruropus_wahli

Glossocephalus_sp

Gammarus_daiberi


Oxycephalus_clausi






Monoporeia_affinis

Gammarid_KML

Hyalella_simplex



Amphithoe_longimana


Orchestia_cavimana


Scypholanceola_sp

Gammarus_oceanicus

Capprellid_KBH

Pallasea_grubei

Epimeria_rubrieques

Orchestia_uhleri

Eurythenes_gryllus



Lysianassoid

Cyamus_erraticus


Lanceola_sayana

Eogammarus_oclairi



Crangonyx_serratus


Micruropus_fixseni

Gammarus_annulatus

Vibilia_propinqua

Micruropus_glaber

Maarrka_wollii





Phronima_sedentaria

Eusirus_cuspidatus

Hyale_nilssoni

Brandtia_lata


Lanceola_loveni

Asellus_aquaticus

Hyperoche_capucinus

Hyalella_sandra





Epimeria_robusta

Paraoroides_sp


Pilbarus_millsi

Epimeria_macrodonta


Lanceola_pacifica

Synopia_sp

Rhachotropis_sp



Synurella_sp

Melita_nitida

Themisto_pacifica


0.11

1

0.55

0.68

0.71

0.93

0.58

0.57

0.82

0.26

0.75

0.77

0.37

0.45

0.08

0.96

0.59

0.93

0.97

0.41

0.05

0.98

1

1

1

0.23

0.61

1

1

0.9

1

1

0.59

0.99

0.6

1

0.41

0.52

0.5

0.94

0.11

0.83

0.97

0.44

1

0.99

1

0.48

0.99

0.3

0.78

1

0.98

0.63

0.63

1

1

1

1

0.62

0.92

0.93

1

0.91

0.96

0.66

1

1

1

1

0.98

0.99

0.27

0.39

0.64

0.2

1

0.61

0.27

0.1

0.560.91

0.99

0.61

0.96

0.08

0.99

0.96

0.09

1

0.5

0.7

0.82

0.47

0.99

1

0.99

0.48

0.85

0.98

0.37

1

0.96

0.64

0.86

1

1

0.99

0.53

0.63

0.99

0.97

0.61

1

1

0.57

0.11

1

0.74

0.13

0.98

1

0.99

1

1

1

0.95

0.27

0.93

1

0.13

0.39

0.96

1

0.95

0.87

0.94

1

1

1

1

1

0.92

0.57

0.43

0.99

0.97

0.96

0.38

0.32

1

0.98

0.13

0.89

1

1

0.46

1

0.43

1

0.97

0.07

0.68

0.5

1

0.2

hyperiidclade 3

hyperiidclade 2

caprellid

hyperiidclade 1

Armadillidium_vulgareCilicaea_spAsellus_aquaticusOrchestia_cavimanaOrchestia_uhleriParhyale_hawaiensis

Synurella_sp

Melita_nitidaMegomaera_subtener

Lycaea_nasuta

Cranocephalus_scleroticusCalamorhynchus_pellucidus

Rhabdosoma_whitei

Streetsia_challengeriOxycephalus_clausi

Leptocotis_tenuirostrisGlossocephalus_milneedwardsi

Tryphana_malmi

Parapronoe_cambelli

Brachyscelus_crusculumBrachyscelus_rapax


Thyropus_sphaeromaPlatyscelus_serratulus

Themisto_japonicaThemisto_pacifica

Hyperoche_capucinus

Hyperia_macrocephalaHyperoche_medusarum

Hyperoche_martinezi

Iulopis_loveni

Phrosina_semilunata_ATLPhrosina_semilunata_PACPrimno_brevidensPrimno_evansi


Cystisoma_gershwinaeCystisoma_pellucida

Phronimella_elongata_ATLPhronimella_elongata_PAC

Phronima_sedentariaPhronima_bucephala

Capprellid_KBHJassa_slatteryi

Cyamus_erraticusCyamus_gracilisCyamus_ovalis

Phronimopsis_spiniferaLestrigonus_schizogeneios

Hyperioides_longipesHyperietta_parviceps

Vibilia_propinquaVibilia_viatrix

Vibilia_antarticaCyllopus_magellanicusCyllopus_lucasii


Lanceola_loveni

Scypholanceola_spScypholanceola_aestiva

Lanceola_sayanaLanceola_pacifica

Mimonectes_loveniScina_borealis


Synopia_sp

Cyphocaris_sp

Gammarid_KML

Rhachotropis_sp

Monoculodes_sp

Gammarid_Tib750

Gammarid_Tib844

Stenothoidae_

Paraoroides_sp

Lysianassoid_

Niphargus_fontanusNiphargus_rhenorhodanensisNiphargus_virei

Eurythenes_gryllus

Abyssorchomene_sp

Hirondellea_dubia

Exhyalella_natalensisHyale_nilssoni



Gammarus_annulatus

Gammarus_duebeniGammarus_oceanicus

Crangonyx_serratus

Amphithoe_longimana

Micruropus_glaber

Hyalella_simplex

Epimeria_rubrieques

Epimeria_reoproi

Uroctena_sp

Epimeria_macrodonta

Epimeria_georgiana

Perthia_sp

Chydaekata_sp

Pilbarus_millsi

Paramelitidae_sp

Brandtia_lata


Iphimediella_rigida



Pallasea_cancellus



Epimeria_similis

Epimeria_robusta



Molina_pleobranchos




Hyalella_azteca

Hyalella_muertaHyalella_sandra

Hyalella_montezuma

Gammarus_lacustris



Ventiella_sulfuris



Dikerogammarus_haemobaphesDikerogammarus_villosusObesogammarus_crassus

Euxinia_maeoticus



Echinogammarus_trichiatusEchinogammarus_ischnus


Crangonyx_floridanusCrangonyx_pseudogracilis

Maarrka_wollii


Eusirus_cuspidatusParamphithoe_hystrix


Micruropus_wahli



Gammarus_daiberiGammarus_tigrinus

Gammaracanthus_aestuariorumGammaracanthus_caspius




Pallasea_grubei

Micruropus_fixseni







Monoporeia_affinis



Ommatogammarus_albinusEulimnogammarus_inconspicuous

Eogammarus_oclairi

Glossocephalus_sp

5370

233

2836

9853

8750

54

1005159

5269

4799

5298

10012

100

24

6594

100

76

4665

5395

100

10075

24

10072

100

29

100

10084

74

53

100

8899

93

33

9821

10094

10085

5843

24

6178

35

10033

11

98100

6314

10093

86

40

42

19

36

18

66

71

28

57

2122

9766

6764

100100

5790

97

45

33

92

8949

8255

10076

83

10041

100

64

10099

95

5029

16

19

68100

Department of Biology ......Convergent evolution and associated character homoplasy are one of the...

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Transcript of Department of Biology ......Convergent evolution and associated character homoplasy are one of the...