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2019), DOI: 10.1111/Syen.12350 Systematic Entomology (2019), DOI: 10.1111/syen.12350 Phylogenomic analysis of seal lice reveals codivergence with their hosts MARÍA SOLEDAD LEONARDI1 ,STEPHANYVIRRUETA HERRERA2,ANDREWSWEET2,3,JAVIERNEGRETE4 and K E V I N P . J O H N S O N 2 1Laboratorio de Biología de Predadores Tope Marinos, IBIOMAR, CCT CONICET– CENPAT, Puerto Madryn, Argentina, 2Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Champaign, Illinois, U.S.A., 3Department of Entomolog, Purdue University, West Lafayette, IN, U.S.A. and 4Instituto Antártico Argentino y Facultad de Ciencias Naturales y Museo de La Plata, La Plata, Argentina Abstract. Lice are considered a model system for studying the process of cospeciation because they are obligate and permanent parasites and are often highly host-specifc. Among lice, species in the family Echinophthiriidae Enderlein (Anoplura) are unique in that they infest mammalian hosts with an amphibious lifestyle, i.e. pinnipeds and the river otter. There is evidence that the ancestor of this group infested the terrestrial ancestor of pinnipeds, which suggests these parasites coevolved with their hosts during the transition to marine environments. However, there has been no previous study inves- tigating the phylogenetic relationships among sucking lice parasitizing seals and sea lions. To uncover the evolutionary history of these parasites, we obtained genomic data for Antarctophthirus microchir Trouessart and Neumann (from two hosts), Antarctoph- thirus carlinii Leonardi et al., Antarctophthirus lobodontis Enderlein, Antarctophthirus ogmorhini Enderlein, Lepidophthirus macrorhini Enderlein, and Proechinophthirus fuctus Ferris. From genomic sequence reads, we assembled > 1000 nuclear genes and used these data to infer a phylogenetic tree for these lice. We also used the assembled genes in combination with read-mapping to estimate heterozygosity and effective population size from individual lice. Our analysis supports the monophyly of lice from pinnipeds and uncovers phylogenetic relationships within the group. Surprisingly, we found that A. carlinii, A. lobodontis,andA. ogmorhini have very little genetic divergence among them, whereas the divergence between different geographic representatives of A. microchir indicate that they are possibly different species. Nevertheless, our phylogeny of Echinophthiriidae suggests that these lice have consistently codiverged with their hosts with minimal host switching. Population genomic metrics indicate that louse effective population size is linked to host demographics, which further highlights the close association between pinnipeds and their lice. Introduction technologies provide the opportunity to simultaneously obtain extremely large datasets for both phylogenomic and popula- A very large fraction of all insects are parasites. Phylogenetic tion genomic approaches (Sweet et al.,2017).Inparticular, studies of insect parasites with respect to their hosts provide because of their relatively small genomes (c. 100–200 Mbp), opportunities to understand the basis of insect diversifcation parasitic lice (Insecta: Phthiraptera) provide an excellent system and specialization. In addition, next-generation sequencing (Clayton et al., 2016) in which to use these large datasets to study both the pattern of diversifcation with respect to Correspondence: María Soledad Leonardi, Instituto de Biología de their hosts and the way in which interactions with the hosts Organismos Marinos, CCT CONICET–CENPAT, Bvd. Brown 2915, PC 9120, Puerto Madryn, Argentina. might infuence population-level processes. Here we use E-mail: [email protected] these datasets to study the process of codiversifcation and © 2019 The Royal Entomological Society 1 2 M. S. Leonardi et al. Table 1. Seal–louse associations of the family Echinophthiriidae 2012). Australian sea lions (Neophoca cinerea Péron) are par- (Anoplura). ticularly at risk, and have been listed as endangered on the IUCN Red List since 2008 (Goldsworthy, 2015). Although some Genus Species Host life-history traits of certain pinniped species, such as small Antarctophthirus callorhini Northern fur seal breeding colonies, may contribute to their low numbers, human carliniia Weddell seala actions have also contributed to their decline (Hamer et al., lobodontisa Crabeater seala 2013). Compared with other aspects of their biology, the phy- mawsoni Ross seal logeny of pinnipeds is relatively well studied and provides an a microchir Steller, Californian, South evolutionary framework in which to understand the evolution Americana,Australiana and New Zealand sea lion of their parasitic lice. Molecular analysis supports the mono- ogmorhinia Leopard seala phyletic origin of the Pinnipedia with a basal split between trichechi Walruses Otarioidea (fur seals and walruses) and Phocoidea (true seals) Latagophthirus rauschi Northern river otter (Arnason et al.,2006).CurrentevidencesuggestsaNorthAmer- Lepidophthirus macrorhinia Elephant sealsa ican origin for pinnipeds. This was followed by an Atlantic dis- piriformis Monk seals persal for phocids and a Pacifc dispersal for otariids into the Echinophthirius horridus Northern true seals southern hemisphere. Coinciding with this scenario, Kim (1985) Proechinophthirus fuctusa a Northern fur seal suggested that pinniped lice have coevolved with the ancestral zumpti Southern fur seals Otarioidea and Phocidae, being present in the terrestrial ancestor aLouse and seal species sampled in this study. of pinnipeds. Therefore, the origin and diversifcation of these lice are likely to be intimately associated with host evolutionary history. However, there have been no prior studies of the phy- effective population size in the sucking lice (Anoplura) of seals logeny of pinniped lice. (Pinnipedia). The primary goal of this study is to analyse the evolutionary Sucking lice are obligate, permanent and haematophagous history of sucking lice parasitizing seals and sea lions, prin- insects, living as ectoparasites in the fur or hairs of their cipally in Patagonia and Antarctica, applying next-generation mammalian hosts. Sucking lice in the family Echinophthiriidae sequencing approaches. We explore the utility of genome Enderlein are unique in that they infest amphibious hosts, such sequencing to resolve the phylogeny of seal lice and to estimate as pinnipeds (walruses, seals and sea lions) and river otters (Dur- demographic parameters of lice from the same genomic data. den & Musser, 1994; Leonardi & Palma, 2013). Other aquatic Finally, we compare the phylogeny of these lice with that of their (e.g. whales, dolphins, manatees) or amphibious (e.g. platy- hosts in a cophylogenetic framework. pus, hippos) mammals do not host lice. The family Echinoph- thiriidae comprises fve genera and 13 species. Genera include Latagophthirus Kim and Emerson (one species) from the North Methods river otter, Proechinophthirus Ewing (two species) from fur seals, Echinophthirius Giebel (one species) from seals in the Genome sequencing northern hemisphere, Lepidophthirus Enderlein (two species) from monk and elephant seals, and Antarctophthirus Enderlein Louse samples were collected with combs or tweezers in the (seven species) from a variety of pinnipeds (Table 1). Antarc- feld from their hosts’ hind fippers and preserved in 96% ethanol tophthirus is the most diverse genus, and most species are highly (see details in Leonardi, 2014). When anaesthetization of seals host-specifc(Durden&Musser,1994).SpeciesofAntarctoph- was needed, the animals were immobilized following routine thirus are associated with a diversity of pinnipeds, including procedures (see details in Wheatley et al.,2006)bypeoplefrom walruses (Odobenidae Allen), Antarctic seals (Phocidae Gray) the Argentinean Antarctic Institute. Collecting lice from the and sea lions (Otariidae Gray). Just as their hosts, these lice prob- fippers provides a reliable proxy for total louse load, and also ably have a terrestrial origin (Kim, 1985). Therefore, these lice reduces host handling time (Leonardi et al.,2018).Antarcticlice evolved many unique morphological, physiological, behavioural were collected in the northern sector of the Danco Coast and 25 and ecological adaptations to cope with the amphibious lifestyle de Mayo Island; lice from Australian sea lions and the northern of their hosts. Some of these adaptations include increased den- fur seal were sampled by Rebecca McIntosh, Phillip Island sity of setae and reduced development time (Kim, 1971; Murray, Nature Parks, Australia, and Christine Fontaine, The Marine 1976; Mehlhorn et al.,2002;Leonardiet al.,2012;Leonardi Mammal Center, U.S.A.; fnally, lice from South American & Lazzari, 2014). These specialized traits, together with host sea lions were obtained from the Parasitological Collection specifcity of these lice, suggest that they coevolved with their at Centro Nacional Patagónico, Puerto Madryn. Before DNA hosts during the colonization of the marine environment (Kim, extraction, each specimen was photographed at the University 1975, 1985; Kim et al., 1975). of Illinois, Urbana-Champaign, as a voucher. Whole lice were Marine mammals such as pinnipeds are more poorly stud- ground up individually (Table S1) in 1.5 mL tubes and genomic ied and generally more threatened compared with terrestrial DNA was isolated using standard protocols and reagents of mammals. One in three species of pinnipeds is threatened com- the Qiagen QIAamp DNA Micro Kit (Qiagen, Valencia, CA, pared with one in fve mammals more generally
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