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Amphipoda): a Eulogy For bioRxiv preprint doi: https://doi.org/10.1101/2020.10.24.353664; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 1 Origin and evolution of the Haustoriidae (Amphipoda): A eulogy for 2 the Haustoriidira 3 4 Running Title: Origin of Haustoriidae 5 6 Zachary B. Hancock*1,2, Hiroshi Ogawa3, Jessica E. Light2,4, Mary K. Wicksten1,2 7 8 1Department of Biology at Texas A&M University 9 2Ecology and Evolutionary Biology Interdisciplinary Program at Texas A&M University 10 3Association for Protection of Marine Communities, 69 Jodoji-shimobanbacho, Sakyo, Kyoto 11 606-8413, Japan E-mail: [email protected] 12 4Department of Ecology and Conservation Biology at Texas A&M University 13 *Corresponding author: [email protected] 14 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.24.353664; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 15 ABSTRACT 16 17 Haustoriid amphipods, despite their ubiquity in coastal sand or mud, have received little recent 18 attention and their systematics and phylogenetics are largely unresolved. Some efforts have been 19 made at classifying the family within the broader Amphipoda, but there is persistent 20 incongruence in its placement among different authors and techniques. Furthermore, there exists 21 no phylogenetic hypothesis of intrafamilial relationships despite the potential for rich 22 biogeographic information to be gained given the specific habitat requirements of haustoriids and 23 their limited dispersal abilities. In this work, we evaluate the competing hypotheses on the 24 phylogenetic position of the Haustoriidae within Amphipoda by examining new and previously 25 published sequences of nearly 100 species across 38 families. We find strong support for the 26 Haustoriidae as basal gammarids, and that other families placed within the parvorder 27 “Haustoriidira” are spread across Amphipoda. The radiation began during the Eocene and may 28 have been driven in North America by the rapid filling of a coastal niche opened by the 29 Chesapeake Bay impact crater. Unlike previous work, we find that the Pacific-endemic genus 30 Eohaustorius is the most basal haustoriid, and that it separated from the rest of the family ~31 31 Mya. Finally, based on ancestral reconstructions, we provide taxonomic recommendations for 32 relationships within Haustoriidae, including the elevation of a new genus, Cryptohaustorius. We 33 conclude by recommending that the “Haustoriidira” be abandoned. 34 35 KEYWORDS: Biogeography, divergence-time, homoplasy, phylogenetics, sand-burrowing, 36 taxonomy bioRxiv preprint doi: https://doi.org/10.1101/2020.10.24.353664; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 37 INTRODUCTION 38 39 Amphipoda is an incredibly diverse order of crustaceans with nearly 10,000 described 40 species (Barnard, 1957; Lowry & Myers, 2017). One such family of amphipods with uncertain 41 affinity, the Haustoriidae, were deemed by J. Laurens Barnard as “perhaps the most interesting 42 group of amphipods” (Barnard, 1969) likely because they are highly morphologically specialized 43 to a fossorial lifestyle. Haustoriids are found on both open and protected beaches around the 44 world but are hypothesized to have originated in the western North Atlantic (Bousfield, 1970). 45 These amphipods have broad, fusiform bodies, lack eye pigmentation, and sport a dizzying array 46 of spines and setae that give them the appearance of a fuzzy, opaque bean (Fig. 1e). They have 47 lost article 4 on their mandibular palp (article 3 is strongly geniculate in compensation) and they 48 are characterized by the absence of dactyls on pereopods 3–7. On gnathopods 1–2, the dactyls 49 have been highly reduced; on gnathopod 1 they are a thin, curved nail, whereas they compose a 50 minute chela on gnathopod 2. Pereopods 3–4 are perhaps the most curious: article 6 forms an 51 expanded cup-like structure that is lined by stout spines for digging through the sediment (except 52 in Eohaustorius spp.; pereopod 4 is a miniature version of pereopod 5). The last three legs are 53 broadly expanded with each article as wide as they are long, and densely lined with comb setae. 54 The posterior of haustoriids are as bushy as the front, and they have evolved powerful uropods 55 with strong apical spines that aid in propelling them through the sand. 56 Lowry & Myers (2013) erected a suborder of Amphipoda, Senticaudata, on the basis of 57 the supposedly synapomorphic robust apical spines on uropods 1 and 2. This grouping includes 58 many diverse and geographically widespread groups, such as the gammarids, talitrids, 59 corophiids, and others. However, Lowry & Myers (2013) argue that the phoxocephalids and bioRxiv preprint doi: https://doi.org/10.1101/2020.10.24.353664; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 60 haustoriids have acquired this trait convergently and are excluded from this suborder. Instead, 61 Lowry & Myers (2017) place the haustoriids in the suborder Amphilochidea, allying them with 62 the pelagic lysianassids, the synopiids, and other fossorial amphipods included within the 63 parvorder Haustoriidira (see Taxonomy in Methods). Verheye et al. (2016) has called into 64 question the usefulness of the robust spines on the uropods for higher level classification, finding 65 that it appears to evolve convergently across many families. 66 The modern taxonomy of the Haustoriidae (as with many amphipod families) was shaped 67 by the morphological work of E.L. Bousfield and J. Laurens Barnard. Bousfield (1965) redefined 68 the family from Stebbing’s (1906) original description, erecting two subfamilies: the 69 Haustoriinae (or the “true” haustoriids) and the Pontoporiinae (previously their own family, the 70 Pontoporiidae). In addition to the two haustoriid genera already recognized (Haustorius and 71 Lepidactylus), Bousfield (1965) described five new genera of haustoriids and redistributed most 72 of the described species at the time between them: Protohaustorius, Acanthohaustorius, 73 Pseudohaustorius, Neohaustorius, and Parahaustorius. After 1965, the only species that 74 remained in the nominal genus Haustorius were H. arenarius, the original type species, and H. 75 canadensis Bousfield, 1962 (Hancock & Wicksten, 2018). These two would be joined later by H. 76 algeriensis Mulot, 1967 from Algeria, H. orientalis Bellan-Santini, 2005 from the 77 Mediterranean, H. jayneae Foster & LeCroy, 1991 from the eastern Gulf of Mexico, H. 78 mexicanus Ortiz et al., 2001 from the state of Veracruz, Mexico, H. galvezi Hancock & 79 Wicksten, 2018 from the western Gulf, and H. allardi Hancock & Wicksten, 2018 from the 80 Mississippi Delta region. Among the haustoriids, the species within Haustorius are the largest by 81 body size, and they tend to inhabit the high intertidal zone on surf-exposed sandy beaches 82 (Hancock & Wicksten, 2018; Hancock et al., 2019). The proposed sister to Haustorius is bioRxiv preprint doi: https://doi.org/10.1101/2020.10.24.353664; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 83 Lepidactylus, which looks remarkably similar to Haustorius except for the lack of an overhang 84 of epimeron 3 (Robertson & Shelton, 1980; Hancock & Wicksten, 2018). Hancock et al. (2019), 85 using four molecular markers, found support for Lepidactylus as sister to Haustorius, but this 86 work only included L. triarticulatus from the Gulf of Mexico and no other genera. 87 The phylogenetic position of the Haustoriidae within the Amphipoda has never been 88 resolved. An early phylogenetic hypothesis was given by Barnard & Drummond (1982) in which 89 they proposed that the Haustorioidea, a superfamily that includes the quintessential fossorial 90 amphipod families (see Taxonomy in Methods), evolved from gammarid ancestors, and that the 91 most basal lineage is the Pontoporeiidae (Fig. 1a). They wrote, “Pontoporeiids are very close to 92 the Pontocaspian gammaroids… but differ in the enfeeblement of the gnathopods and the 93 somewhat enlarged mandibular molars with relatively weaker triturative states and the loss of 94 coxal gill 7” (Barnard & Drummond, 1982). Barnard & Drummond (1982) united the remaining 95 haustorioids by the presence of the “haustoriid-like” pereopod 5: greatly expanded and heavily 96 spinated. Those that did not then develop the “haustoriid-like” antenna were proposed to form a 97 clade consisting of the Urothoidea, Platyischnopidae, and Condukiidae (Barnard & Drummond, 98 1982). Those that obtained the haustoriid antennae were then divided into two clades: 1) those 99 that lack a mandibular palp and glassy spines (the Phoxocephalidae) and 2) those with: the 100 Haustoriidae, Phoxocephalopsidae, Zobrachoidae, and the Urohaustoriidae. 101 A more recent phylogeny (Lowry & Myers, 2017), based again on morphological 102 character states, proposed that the Haustoriidae are sister to the enigmatic Condukiidae, a family 103 endemic to Australia, while retaining the basal position of the Pontoporeiidae (with the addition 104 of an even more basal group, the Priscillinidae).
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