Global Parasite and Rattus Rodent Invasions

Home , Black rat, Polynesian rat, Rattus, Trypanosoma lewisi

Integrative Zoology 2015; 10: 409–423 doi: 10.1111/1749-4877.12143

1 REVIEW 1 2 2 3 3 4 4 5 5 6 6 7 Global parasite and Rattus rodent invasions: The consequences 7 8 8 9 for rodent-borne diseases 9 10 10 11 11 12 12 13 Serge MORAND,1,2 Frédéric BORDES,3 Hsuan-Wien CHEN,4 Julien CLAUDE,3 Jean-François 13 14 5,6 5 7 7 3,8 14 15 COSSON, Maxime GALAN, Gábor Á CZIRJÁK, Alex D GREENWOOD, Alice LATINNE, 15 16 Johan MICHAUX1,8 and Alexis RIBAS9 16 17 17 1 18 Centre National de la Recherche Scientifque (CNRS)-Centre de coopération Internationale en Recherche Agronomique pour le 18 19 Développement (CIRAD) Animal et Gestion Intégrée des Risques, Centre d’Infectiologie Christophe Mérieux du Laos, Vientiane, 19 20 Lao PDR, 2Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand, 3Institut des 20 21 Sciences de l’Evolution, Centre National de la Recherche Scientifque (CNRS)-Université de Montpellier-Institut de Recherche 21 22 pour le Développement (IRD), Montpellier, France, 4Department of Biological Resources, National Chiayi University, Chiayi 22 23 City, Taiwan, China, 5Institut National de la Recherche Agronomique (INRA), Centre de Biologie et de Gestion des Populations, 23 24 Baillarguet, France, 6Institut National de la Recherche Agronomique (INRA), UMR Biologie et Immunologie Parasitaire Agence 24 25 25 Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du Travail ses, Maisons-Alfort, France, 7Leibniz Institute 26 26 for Zoo and Wildlife Research. Department of Wildlife Diseases, 10315 Berlin, Germany, 8Conservation Genetics Unit. University 27 27 9 28 of Liège 4000 Liège, Belgium and Biodiversity Research Group, Faculty of Science, Udon Thani Rajabhat University, Udon Thani, 28 29 Thailand 29 30 30 31 Abstract 31 32 32 33 We summarize the current knowledge on parasitism-related invasion processes of the globally invasive Rattus 33 34 lineages, originating from Asia, and how these invasions have impacted the local epidemiology of rodent-borne 34 35 diseases. Parasites play an important role in the invasion processes and successes of their hosts through multi- 35 36 ple biological mechanisms such as “parasite release,” “immunocompetence advantage,” “biotic resistance” and 36 37 “novel weapon.” Parasites may also greatly increase the impact of invasions by spillover of parasites and other 37 38 pathogens, introduced with invasive hosts, into new hosts, potentially leading to novel emerging diseases. An- 38 39 other potential impact is the ability of the invader to amplify local parasites by spillback. In both cases, local 39 40 fauna and humans may be exposed to new health risks, which may decrease biodiversity and potentially cause 40 41 increases in human morbidity and mortality. Here we review the current knowledge on these processes and pro- 41 42 pose some research priorities. 42 43 43 Key words: biological invasion, immunocompetence, parasite release, spillback, spillover 44 44 45 45 46 46 47 47 48 Correspondence: Serge Morand, Centre d’Infectiologie INTRODUCTION 48 Christophe Mérieux du Laos, PO Box 3888, Samsenthai Road, 49 Emerging infectious diseases share several patterns 49 Vientiane, Lao PDR. 50 and processes with free-living invasive organisms. How- 50 51 Email: [email protected] 51

1 ever, host–parasite (in a broad sense including macro colonized ecosystems in different ways (Courchamp et 1 2 microparasites and microparasites) interactions are more al. 2003; Banks & Hughes 2012) and can also have eco- 2 3 complex due to interactions operating at the level of the nomic impacts. Moreover, these species display suffi- 3 4 individual (e.g. life-history trait, defense and virulence), cient ecological differences that they would be expected 4 5 population (e.g. dynamics and disease regulation), com- to interact differently with local small mammal commu- 5 6 munity (e.g. co-interactive networks of parasitism, com- nities (Courchamp et al. 2003; Singleton et al. 2007). 6 7 petition and predation) and ecosystem (e.g. parasites in All these Rattus species have radically and explosive- 7 8 food webs, and disease spread within habitat connectivi- ly expanded their geographic range as a consequence of 8 9 ty). human activities. Interestingly, all of these rodents orig- 9 10 Parasites play an important role in the invasion pro- inated in Asia, and they can be found in sympatry in 10 11 cesses and successes of their hosts through multiple bio- many localities, even far from their original distribution 11 12 logical mechanisms, such as “parasite release” (Torchin (Bastos et al. 2011; Blanks & Hugues 2012; Lack et al. 12 13 13 et al. 2003), “immunocompetence advantage” (Møller 2012) due to their synanthropic behavior (Khlyap & 14 14 & Cassey 2004), “biotic resistance” (Britton 2012), and Warshavsky 2010; McFarlane et al. 2012). As these rat 15 15 “novel weapon” (Strauss et al. 2012), among others species are closely associated with humans, the timing 16 16 (Prenter et al. 2004; Bell et al. 2009; Dunn 2009; Kel- of their invasion is related to current and historical glob- 17 17 ly et al. 2009; Morand et al. 2010). Parasites may also al trade. 18 greatly increase the impact of invasions through spill- 18 Rodents are recognized as hosts of at least 60 zoo- 19 over of parasites/pathogens into new hosts, potential- 19 notic diseases that represent a serious threat to human 20 ly leading to novel emerging diseases and/or the emer- 20 21 gence of already known diseases in new geographic health (Meerburg et al. 2009; Luis et al. 2013; Chai- 21 22 areas (Hulme 2014). A second local potential impact is siri et al. 2015). Historically, Asian rodents of the ge- 22 23 the ability of the invader to amplify local parasites by nus Rattus have been implicated in the emergence and 23 24 spillback. Spillover and local acquisition of parasites spread of infectious diseases of importance to human 24 25 and pathogens have important consequences for ecolog- health such as plague, murine typhus, scrub typhus, lep- 25 26 ical systems, wildlife and domestic species (Wood et al. tospirosis and hantavirus hemorrhagic fever, among oth- 26 27 2012). In both cases, local fauna and humans may be ers (Kosoy et al. 2015). They can cause considerable 27 28 exposed to new or elevated health risks (Hatcher et al. economic loss (Stenseth et al. 2003; Singleton et al. 28 29 2012). 2010; John 2014) and have great impact on biodiversity 29 30 30 Few host–parasite systems permit an overall view of (Atkinson 1985; Lowe et al. 2001; Wyatt et al. 2008). 31 31 the consequences of biological invasions at multiple lev- Our aims are to review the ecological and biologi- 32 32 els of biological organization, at different global scales cal knowledge on Rattus invaders and the consequences 33 33 and linking risks of emerging diseases. Invasive rodents of their invasion success on rodent-borne diseases and, 34 34 are one of the few models that allow such a comprehen- based on this review, to emphasize gaps in knowledge 35 35 sive scalable analysis to be performed. Among the nu- and recommend some future research priorities. 36 36 merous species within Rattus (66 species according to 37 37 Musser & Carlton 2005), the Norway or brown rat Rat- 38 PARASITES IN THE INVASION 38 tus norvegicus (Berkenhout, 1769), the black or roof rat 39 39 Rattus rattus (Linnaeus, 1758), and the Asian black rat PROCESSES: CAUSES AND LIKELY 40 40 Rattus tanezumi Temminck, 1844 have colonized urban 41 CONSEQUENCES 41 ecosystems globally (Aplin et al. 2011). A fourth inva- 42 42 sive species, the Pacifc rat Rattus exulans (Peale, 1848) Biotic invasions are often compared to epidemics as 43 43 is limited to tropical Asia-Pacific areas. Finally, oth- several important factors in disease epidemiology are 44 44 er species in the group [Rattus argentiventer (Robinson common to invasion biology (Mack et al. 2000): the 45 45 and Kloss, 1916], Rattus nitidus (Hodgson, 1845) and chance of establishment, the minimum population size 46 46 Rattus tiomanicus (Miller, 1900) have shown an expan- necessary for establishment in the invaded habitat, the 47 47 sion associated with human activities but to a less geo- population growth and the fate of interacting species in 48 48 graphical extent (Aplin et al. 2003). It is well known the new range (Drake 2003). These factors are the core 49 49 that, once introduced, all these species can strongly in- of the invasion process, which has been defned as a se- 50 50 teract with indigenous fauna and fora, and can alter the quence of 3 steps: introduction, initial establishment and 51 51

1 spread (Williamson 1996; Kolar & Lodge 2001; Facon parasites in the introduced range; any co-introduced par- 1 2 et al. 2006; Fig. 1). asites may be useful for the control of native hosts by 2 3 The first step, introduction, is associated to the dis- spillover, which may have few opportunities for invest- 3 4 persal ability of the species, although introduction is ment in defense, especially if living on islands (Hoch- 4 5 mainly dependent on human activities. The second step, berg & Møller 2001). Fourth, in the absence of parasites 5 6 initial establishment, depends mainly on the fate of in- in the invaded localities, invasive species can reallocate 6 7 teraction with the local environmental characteristics. energetic resources from unnecessary costly defenses 7 8 The last step, spread or population growth, clearly de- into ftness (e.g. reproduction) and growth, leading ulti- 8 9 pends on the biological characteristics of invasive spe- mately to spread and establishment success through in- 9 10 cies and of the effects of competition, predation and par- creased competitive ability (Blossey & Nötzold 1995). 10 11 asitism, which may ultimately affect its evolutionary The parasite release hypothesis was proposed as an 11 12 adaptation to the invaded habitats (Facon et al. 2006). ecological mechanism to explain the success of intro- 12 13 13 Several hypotheses for parasite or disease-related duced species, as the introduced species may have lost 14 14 mechanisms have been proposed to explain the success their parasites when invading new habitats. The intro- 15 15 of invaders over endemic species (summarized in Fig. duced species have a competitive advantage over local 16 16 1 and Table 1): parasite release (i.e. enemy release), im- species because they are released from control by their 17 17 munocompetence advantage, the apparent competition natural enemies (Elton 1958; Keane & Crawley 2002; 18 18 due to co-invasive parasite spillover (i.e. novel weapon) Torchin et al. 2003). Nevertheless, several studies indi- 19 19 and the reallocation of enegertic resources following the cate that most of the parasite species of an invasive spe- 20 20 loss of parasites. cies are either left in their native area, are lost or can- 21 21 In the invasion process, hosts harboring a high di- not establish in the invaded habitat (Dobson & May 22 1986; Pisanu et al. 2009; Dozières et al. 2010; Marzal 22 23 versity of parasites in their native locations have a four- 23 fold advantage. First, they lose a great number of par- et al. 2011). Indeed, in the case of parasites with com- 24 plex lifecycles and vector-borne pathogens, the miss- 24 25 asites and pathogens in their introduced range and are 25 released from their control (Torchin et al. 2003). The ing intermediate hosts and vectors in the new invaded 26 habitats could lead to a decrease in parasite diversity of 26 27 main parasites missing are those that require an interme- 27 diate host for transmission (for house mice see Single- the introduced species. Finally, associated invasive par- 28 asite species may fail to infect new local host species 28 29 ton et al. 2005). Second, they have evolved strong im- 29 mune defenses in their natural range (Bordes & Morand as many parasites may develop only in phylogenetical- 30 ly-related host species (Pisanu et al. 2009). Mitchell and 30 31 2009), which may subsequently confer a better capacity 31 to control parasites that they may acquire by spillback Power (2003) and Torchin et al. (2003) fnd that parasit- 32 ism is signifcantly reduced in organisms in their intro- 32 33 in the introduced range. Third, they do not lose all their 33 34 34 35 35 36 36 37 37 38 38 39 39 40 40 41 41 42 42 43 43 44 44 45 45 46 46 47 47 48 48 49 Figure 1 Parasite-related traits (native lo- 49 50 cality), mechanisms and consequences of 50 51 invasion. 51

1 Table 1 Hypotheses related to disease-causes and consequences of biological invasion with potential tests 1 2 2 Hypothesis Mechanism Test 3 3 4 Causes Enemy release/parasite release Loss of parasites, with lowering Parasite species and host genetic 4 genetic diversities and/or missing comparisons in native, historical and 5 vectors and intermediate hosts in newly invaded localities 5 6 invaded localities 6 7 Immunocompetence Strong immunocompetence that Higher immunocompetence and 7 8 advantage to face biotic copes with local parasites immunogenes diversity in native 8 9 resistance compared to invaded territories; 9 10 correlation between level of 10 immunocompetence and parasite 11 11 diversity 12 12 13 Novel weapon Co-invasive parasites infecting Higher virulence of parasites in invaded 13 14 (i.e. apparent competition due susceptible hosts in the invaded communities than in invasive host; 14 15 to parasite spillover to face localities lower or absent immunity against 15 biotic resistance) the parasite in the susceptible hosts 16 compared to the invading host 16 17 17 Consequences Parasite spillover Spread of co-invasive pathogens in Molecular and serological surveys 18 humans or in local reservoirs 18 19 (emerging zoonoses) 19 20 Parasite spillback Amplifcation of local pathogens in Molecular and serological surveys 20 21 the newly invaded territories 21 22 (outbreaks of zoonoses) 22 23 Loss of dilution effect Spread of co-invasive parasites Molecular and serological surveys 23 24 in low species rich invaded 24 25 communities (such as islands or 25 26 disturbed habitats) 26 27 Higher reproductive success Due to costs of the infammatory Measuring the infammatory response 27 28 and low infammatory immune response and trade- and reproductive traits of the invading 28 response in invaders as a off with other life history traits, species (both in native and invaded 29 29 consequence of the parasite invaders releasing their pathogens territories) and in resident hosts 30 release hypothesis can invest less in infammatory 30 31 response, more in reproduction 31 32 Strong humoral Encountering new pathogens is Measuring the humoral immune 32 33 immunocompetence in invader more effective to fght with a response of the invading species (both 33 34 species, as a consequence of less costly immune branch (e.g. in native and invaded territories) and in 34 35 immune investment and/or humoral immune system) resident hosts 35 of using less costly immune 36 responses 36 37 37 38 38 39 39 40 40 41 41 42 duced range, supporting the parasite release hypothesis, hosts having evolved strong immune defenses are then 42 43 which might explain the success of introduced species prime candidates for successful invasion (Lee & Klas- 43 44 (Clay 2003), through reallocating the resources towards ing 2004; Møller & Cassey 2004). However, the immu- 44 45 reproduction, growth or dispersal. nocompetence advantage hypothesis has not been thor- 45 46 Among the traits that favor the establishment and oughly investigated for invasive rodents (Morand et al. 46 47 spread of invasive species in new localities are those 2010). 47 48 that help in coping with parasitism (i.e. immunity). The Species-poor communities, presenting vacant nich- 48 49 immunocompetence advantage hypothesis was proposed es within communities, both for hosts and for their par- 49 50 for introduced plants and animals and suggests that asites, may also provide opportunities for the settlement 50 51 51

1 and spread of biotic invaders (Elton 1958). The vacant R. norvegicus originated presumably from China 1 2 niches hypothesis suggests that species-poor communi- (Nowak 1999; Song et al. 2014) and expanded world- 2 3 ties do not offer biological resistance to invasion. This wide with more recent European trade. It signifcantly 3 4 would explain why insular communities are so prone to colonized Europe during the 18th century (Vigne & Vil- 4 5 invasion. lié 1995), and reached North America and Africa soon 5 6 Less investigated are the consequences of invasion after (Nowak 1999; Song et al. 2014). Norway rats are 6 7 for the emergence or spread of diseases either by spill- mostly restricted to urban areas with high human den- 7 8 over (co-invasive pathogen) or by spillback (amplifi- sity and domestic animals but few are found in wild ar- 8 9 cation of a local pathogen by the invader; Kelly et al. eas, whereas in the cooler regions they can be found in 9 10 2009; Dunn et al. 2012). One example of a novel weap- grassland and marshy rural areas such as in the south- 10 11 on, among others, concerning rodents is the introduction ern USA (Glass et al. 1989) or Mediterranean (Chey- 11 12 of the grey squirrel (Sciurus carolinensis Gmelin, 1788), lan 1984) and Oceanic islands (Abdelkrim et al. 2005). 12 13 which originated from North America but was introduced Based on a worldwide sampling and molecular analy- 13 14 to the UK and has led to local extinction of the native red sis, Song et al. (2014) suggest that the origin of the spe- 14 15 squirrel (Sciurus vulgaris Linnaeus, 1758) because of the cies occurred more than 1 million years ago in Southern 15 16 co-introduced squirrel poxvirus, a highly pathogenic vi- China, and that the species started to colonize the world 16 17 rus for red squirrels (Tompkins et al. 2003). (Pacifc Islands, Africa, North America) during the last 17 18 The study of these causes and consequences of inva- 2 centuries from the populations that were introduced 18 19 sion necessitate investigation of immunology (genes, and established in Europe. Lack et al. (2013) have de- 19 20 structure and function) of the invasive species in its na- tected high gene fow among established populations in 20 21 tive distribution and in the invaded localities, togeth- the USA, suggesting high connectivity among Norway 21 22 er with its sympatric congeners (with which the chanc- rat populations due to the recent colonization. 22 23 es of sharing parasites are high). Spillover presents the R. rattus and R. tanezumi can be found globally and 23 24 advantage to increase the invaders’ competitive ability in most type of habitat. They have invaded a large range 24 25 with local communities (i.e. the novel weapon hypothe- of anthropogenic and natural environments, where they 25 26 sis) and to favor the ultimate spread of the invasive spe- are likely interacting with a large range of wild and do- 26 27 cies (Bell et al. 2009; Strauss et al. 2012). mestic animals (Goodman 1995; Harris et al. 2006; 27 28 Hoberg 2010; Wells et al. 2014a,b). The origin of the 28 29 THE RATTUS INVADERS: black rat is still debated. Nowak (1999) indicate a Ma- 29 30 laysian origin, Musser and Carlton (2005) an origin 30 31 EVOLUTIONARY AND RECENT from the Indian Peninsula, and Aplin et al. (2011) mul- 31 32 DISTRIBUTION tiple lineages and geographic origins of black rats from 32 33 South and Southeast Asia. Among the lineages, 4 have 33 34 The Rattini is an evolutionarily diverse group and been described as separate species, the black rat R. rat- 34 35 progress has been made in understanding the relation- tus and the Asian black rat R. tanezumi. R. rattus orig- 35 36 ship and evolution of this group (Robins et al. 2008; inated in South Asia and dispersed to Europe along the 36 37 Pagès et al. 2013). According to the phylogenetic analy- Silk Road, and other trade routes that have been report- 37 38 ses of Robins et al. (2008), the deepest divergence with- ed from archeological sites as early as 1500 BC from the 38 39 in Rattus occurred 3.5 Ma with the separation of the Near-East Levant (Near East regions; Ervynck 2002), 39 40 New Guinean endemic Rattus praetor (Thomas, 1888) and to Madagascar, South Arabia and East Africa with 40 41 and Asian lineages from a common ancestor. The R. the Indo-Pacific trade (Tollenaere et al. 2010). It later 41 42 norvegicus lineage diverged from other Asian lineages spread worldwide with modern European trade (Aplin 42 43 2.9 Ma. Other date estimates suggest a younger age for et al. 2011). Black rat populations in the USA were like- 43 44 the species ranging from 0.44 to 2.35 Ma (Song et al. ly founded by a few related lineages (Lack et al. 2013), 44 45 2014). The earliest fossils of the R. norvegicus lineage whereas complex invasion pathways have occurred in 45 46 are of about 1.2 to 1.6 Ma (Song et al. 2014). The study Africa and Madagascar, with multiple introductions 46 47 of Robins et al. (2008) suggests that R. exulans lineage from different source populations (Konecny et al. 2013; 47 48 separated 2.2 Ma from the ancestor of the sister species Brouat et al. 2014). R. tanezumi originated in South- 48 49 R. rattus and R. tanezumi. These last 2 species, R. rattus eastern Asia and invaded several localities of South and 49 50 and R. tanezumi, diverged 0.4 Ma from a common an- North America, South Africa and Australia (Aplin et al. 50 51 cestor. 51

1 2011). Both R. rattus and R. tanezumi were identifed in eases in their original distributions (Palmeirim et al. 1 2 coexistence in California (Aplin et al. 2011; Conroy et 2014; Morand et al. 2015). These attributes make them 2 3 al. 2013). In mainland Southeast Asia, R. tanezumi, R. good candidates for testing related parasite invasion hy- 3 4 norvegicus and R. exulans have been found living to- potheses (Table 2). 4 5 gether in households (Morand et al. 2015). 5 Parasite release 6 R. exulans originated from insular Southeast Asia, 6 7 potentially from the island of Flores (Thomson et al. One prediction of the parasite release hypothesis is 7 8 2014), but it remains unclear how the Pacifc rat invaded that parasite species richness should be highest in its 8 9 mainland Southeast Asia (the Indochina) and other parts host’s ancestral centre of origin, which is hypothesized 9 10 of insular Southeast Asia (such as the Philippines). Pa- to be South Asia, Southeast Asia and Southern China for 10 11 cifc rat dispersal has been used to model the history of invasive Rattus (Robins et al. 2008; Aplin et al. 2011). 11 12 Polynesian settlement, as this animal travelled with an- At a global scale, Wells et al. (2014b) observed that 12 13 cestral Polynesians when they dispersed throughout the the total numbers of parasite species were considerably 13 14 Pacifc (Matisoo-Smith & Robins 2004). Archaeological higher in invaded biogeographic realms for R. rattus and 14 15 records of the Pacifc rats, outside their presumed origi- R. norvegicus than in their native Oriental realm. Esti- 15 16 nal distribution, dated their presence from around 4000 mates of parasite species richness of R. norvegicus were 16 17 BP in East Timor, 3000 BP in west Polynesia to 1000 higher in the Palearctic region than in the Orient, where 17 18 BP in south Polynesia (Anderson 2008). New Zealand the host genus Rattus originated and diversifed. Neither 18 19 was also recently colonized by both rats and humans (Ir- rodent species exhibited differences in their overall par- 19 20 win et al. 1990). However, R. exulans was replaced in asite species richness. These observations suggest that a 20 21 many localities in New Zealand by the more recent in- high number of parasite species, through spillback, have 21 22 troduction of R. rattus, R. norvegicus and Mus musculus been acquired by both rat species during their coloniza- 22 23 Linnaeus, 1758 with the European settlement in the past tion history. 23 24 24 200 years (Atkinson 1985; Roberts 1991b). At a regional scale, Goüy de Bellocq et al. (2002) in- 25 25 The historical routes of invasion of the Pacifc rat are vestigated the helminth community structures of rodents 26 26 then relatively clear. However, new invasions from in- in the Mediterranean area. They demonstrated that there 27 27 sular Southeast Asia have recently occurred, with pop- was a signifcant decrease of helminth species richness 28 28 ulations of Pacifc rats established in Taiwan Island and in R. rattus in relation to geographical distances from 29 29 the Ryukyu islands of Japan (Motokawa et al. 2001). invaded Mediterranean islands to the mainland. A strong 30 30 Therefore, new invasion threats still exist for all the Pa- positive correlation was also found between the total 31 cific areas, including the South Japan islands, Austra- 31 32 lia, New Zealand, New Caledonia and French Polynesia 32 33 (Russell et al. 2008). There is also concern about the in- 33 34 vasion of the northern part of Indochina as R. exulans is 34 35 currently absent from small villages in north Laos (Mo- 35 36 rand et al. 2015), although it is present in large cities 36 37 such as Luang Prabang (Promkerd et al. 2008). In main- 37 38 land Southeast Asia, R. exulans is found mostly in hous- 38 es within villages (Morand et al. 2015). However, in in- 39 sular Southeast Asia, it can be found in natural habitats, 39 40 mostly forest (Roberts 1991b). 40 41 41 42 PARASITE AND DISEASE-RELATED 42 43 43 44 INVASION PROCESSES IN INVASIVE 44 45 RATTUS 45 46 46 47 Invasive Rattus spp. are synanthropic species; that is, 47 48 living in close associations with humans although they Figure 2 Helminth species richness of the Pacifc rat, Rattus 48 49 can also be found in undisturbed habitats. They are also exulans, in its putative native region (insular Southeast Asia) 49 50 hosts for numerous parasites and agents of zoonotic dis- and invaded range Mainland Southeast Asia and Pacific is- 50 51 lands. 51

1 Table 2 Some examples of the effects and consequences of parasites on the success and impacts of invasion by Rattus invaders 1 2 2 Effect/consequence Host–parasite system Locality, references 3 3 Parasite release Rattus rattus/helminths Mediterranean mainland and islands, Goüy de 4 4 Bellocq et al. (2002) 5 5 6 Rattus exulans/helminths New Zealand and Polynesian islands, Roberts 6 (1991a) 7 7 8 Parasite spillover Rattus rattus to humans and local rodents/Yersina Worldwide, Gage & Kosoy (2005) 8 9 pestis (plague) 9 10 Rattus spp. to humans/Bartonella Worldwide, Bai et al. (2007), Hayman et al. 10 11 (2013) 11 12 Rattus norvegicus to humans/Seoul hantavirus Worldwide, Lin et al. (2012) 12 13 Rattus spp. to primates/Trypanosoma lewisi Brazil, Maia da Silva et al. (2010) 13 14 Rattus spp. to Acomys johannis/Trypanosoma Niger, Dobigny et al. (2011) 14 15 lewisi 15 16 16 Rattus rattus to Peromyscus maniculatus/Trichuris Islands in USA, Smith & Carpenter (2006) 17 muris 17 18 18 Rattus spp. to humans/Angiostrongylus Brazil, Monte et al. (2012), Spratt (2015) 19 19 cantonensis 20 20 21 21 22 Parasite spillback Rattus exulans/Orientia (scrub typhus) Taiwan, China, Kuo et al. (2011) 22 23 Rattus spp./livestock/Coxiella burnetii (Q fever) The Netherland, Reusken et al. (2011) 23 24 24 25 25 Novel weapon Rattus rattus/Rattus macleari (endemic Christmas Christmas island, Wyatt et al. (2008) 26 Island rat)/Trypanosoma lewisi 26 27 27 28 28 29 29 30 30 31 number of nematode species recorded in R. rattus pop- In the mid-14th century, one-third of the European hu- 31 32 ulations and the size of islands. These findings are in man population died from plague, of which black rats 32 33 strong accordance with the parasite release hypothesis. were assumed to be the source. The third pandem- 33 34 Few studies have been devoted to parasites of R. ex- ic plague started in China and spread around the world 34 35 ulans in its original distribution and its invasive distri- via ships carrying rats infested with Yersinia pestis and 35 36 bution (Roberts 1991a,b; Hasegawa & Syafruddin 1995; imported into San Francisco in 1899 (Gage & Kosoy 36 37 Palmeirim et al. 2014). When investigating the data col- 2005). The invasive associated strains of Y. pestis fur- 37 38 lected in Southeast Asia (mainland and insular) and Pa- ther established themselves in the local rodent commu- 38 39 cific islands, one can show that there is a decrease in nities (Cully et al. 2010). 39 40 parasite species richness, at least for nematodes, from A second example concerns Seoul hantavirus, which 40 41 insular Southeast Asia (its putative area of origin) com- causes hemorrhagic fever in humans. Seoul hantavirus 41 42 pared to mainland Southeast Asia and the Pacific Is- originated in Asian Rattini rodents followed by world- 42 43 43 lands (invaded areas; Fig. 2), which supports the South- wide expansion by Norway rats within the past few cen- 44 44 east Asian insular origin of R. exulans (Thomson et al. turies (Lin et al. 2012; Plyusnina et al. 2012). 45 45 2014), the parasite release hypothesis and parasite spill- Bartonella strains have also been shown to evolve 46 back. 46 47 and diversify in Southeast Asia and further to dissemi- 47 48 Parasite spillover nate worldwide with R. rattus and R. norvegicus (Ellis 48 49 et al. 1999; Hayman et al. 2013). Another study showed 49 The best-known example of spillover by rats is the that Bartonella genotypes identifed in R. rattus in Ban- 50 plague, frst from gerbils to Rattus (Schmid et al. 2015). 50 51 gladesh are identical to those observed from rats in Eu- 51

1 rope, Israel and the USA (Bai et al. 2007). Invasive Rat- back of local parasites from wild or domestic animals. 1 2 tus also introduced borreliosis on the island of Madeira 2 Novel weapon 3 in Portugal (Matuschka et al. 1994). 3 4 Spillover cases may also include parasitic protists. Several studies have been able to demonstrate that a 4 5 For example, Dobigny et al. (2011) found Trypanosoma pathogen co-introduced with an invasive host pushed 5 6 lewisi Gruby, 1843 in black rats in Niger and in native invaded host populations to extinction (Strauss et al. 6 7 African Acomys johannis Thomas, 1912, which suggests 2012). These studies refer to the extinction of endem- 7 8 spillover from R. rattus to the native rodent species. ic Hawaiian birds following the introduction of mosqui- 8 9 Macroparasites like helminths also spilled over. toes and avian malaria, and the replacement of the red 9 10 Smith and Carpenter (2006) evaluate the spillover of squirrel by the invasive grey squirrel carrying squirrel- 10 11 helminth parasites from introduced black rats (R. rattus) pox virus (see Strauss et al. 2012 and references there- 11 12 to native deer mice [Peromyscus maniculatus (Wagner, in). 12 13 1845)] on California Channel Islands. Whereas 40 gen- Wyatt et al. (2008) provide molecular evidence for 13 14 era of helminths are known to parasitize deer mice in such an effect of T. lewisi emerging in endemic Rattus 14 15 North America, only 5 genera occur in the Channel Is- macleari (Thomas, 1887) (Christmas Island rats) after 15 16 lands, and one of these, the nematode Trichuris muris the introduction of black rats. The authors demonstrate 16 17 (Schrank, 1788), was introduced by the black rat. The the absence of trypanosome infection in endemic rats 17 18 nematode Angiostrongylus cantonensis (Chen, 1935), collected prior to the introduction of black rats but the 18 19 the rat lung worm, which causes eosinophilic meningo- presence of the parasite after the introduction using tis- 19 20 encephalitis in humans through spillover, is thought to sue collections from museum specimens. 20 21 21 have originated in Southeast Asia. This nematode dis- The invasive Y. pestis in USA also impacted the local 22 22 persed across several Pacifc islands, Asia, Australia, Af- rodent communities, where the induced mortality de- 23 23 rica, some Caribbean islands and, most recently, in the pended on susceptibility and resistance of rodent spe- 24 24 Americas through the dispersal of R. rattus and R. nor- cies. Some species have undergone devastating mortal- 25 25 vegicus (Monte et al. 2012; Tokiwa et al. 2012) and the ity, such as black-prairie dogs [Cynomys ludovicianus 26 26 invasion of the terrestrial snail Achatina fulica (Férus- (Ord, 1815); Cully et al. 2010)]. 27 sac, 1821), which acts as an intermediate host (Thiengo 27 28 et al. 2012). Immmunogenetics and immunocompetence 28 29 29 Few immunoecological or immunogenetics studies 30 Parasite spillback 30 have been devoted to invasive rodents and White and 31 31 One example of parasite spillback is the Q fever. Fol- Perkins (2012) emphasize the gap between advances in 32 32 lowing its outbreak in the Netherlands in 2007–2010, theory and performance of empirical studies. 33 the occurrence of the agent Coxiella burnetii in com- 33 The relaxed parasite selection on invasive species is 34 mensal rats was investigated (Meerburg & Reusken 34 expected to lead to changes in the immune system (Hor- 35 2011; Reusken et al. 2011). The bacteria were detected 35 rocks et al. 2011), with reduced variability in immuno- 36 in both brown and black rats, suggesting that rats might 36 genes. Most immunogenetic studies of rodents have ex- 37 represent reservoirs contributing to maintenance and 37 amined major histocompatibility complex (MHC) genes. 38 transmission of the bacteria (Reusken et al. 2011). The 38 However, invasive Rattus have not been the main focus 39 relative importance of rodents in the Q-fever pathway 39 of study (see Goüy de Bellocq et al. (2008), for which 40 transmission deserves more investigation (Meerburg & 40 no invasive rodents were analyzed). Parasite-mediated 41 Reusken 2011). 41 selection maintains MHC polymorphism at both inter- 42 Another study focuses on R. exulans, which recent- 42 43 specifc and intraspecifc levels in rodents with high par- 43 ly invaded localities in Taiwan, China. Kuo et al. (2011) asite species diversity being associated with high levels 44 demonstrate that this invasion contributed to the spread 44 45 of MHC genetic diversity (Goüy de Bellocq et al. 2008; 45 of scrub typhus, originally present on this island (Kelly Pilosof et al. 2014). 46 et al. 2009). 46 47 The study of Pilosof et al. (2014) on MHC diversi- 47 48 Wells et al. (2014b) show that both globally invasive ty in murine rodents from Southeast Asia may help in 48 49 R. rattus and R. norvegicus have high overall parasite testing 2 predictions: (i) hosts having evolved strong 49 50 species diversity outside their geographical origins (i.e. immune defense in their native range, due to high par- 50 51 the Orient). This finding suggests high levels of spill- asite pressures, should show successful invasion capac- 51

1 1 2 2 3 3 4 4 5 5 6 Figure 3 Positive linear relationship be- 6 7 tween genetic diversity at the major histo- 7 8 compatibility complex and helminth spe- 8 cies richness for common murine rodents 9 9 species of mainland Southeast Asia. Pos- 10 10 itive residual values suggest high immu- 11 11 nocompetence such as observed for the 12 12 global invader Rattus tanezumi, native of 13 Southeast Asia. Negative residual values 13 14 suggest low immunocompetence, such as 14 15 observed in Rattus exulans, which is sup- 15 16 posedly originated from insular Southeast 16 17 Asia. 17 18 18 19 19 20 20 21 ity; and (ii) invasive hosts in the invasive range should notype of the invader and congener rodent species. Ro- 21 22 show reduced level of immune defense. Plotting allel- dents, especially rats and mice, are important models for 22 23 ic diversity against parasite species diversity (both con- infectious biology or for medical immunology. Despite 23 24 trolling for sampling biases) confrmed both predictions the existing immunological toolkits for these species, we 24 25 (Fig. 3). R. tanezumi, from mainland Southeast Asia, do not have information about their immunocompetence 25 26 showed high positive residual values of allelic diversity in the wild, especially along various environmental gra- 26 27 (controlled for parasite load) in its original range, mean- dients. Recent studies showed that the immunocompe- 27 28 ing that it evolved high diversity at MHC genes that has tence of the rodents varies between captive and free-liv- 28 29 helped it succeed as a global invader. R. exulans, from ing individuals, both at intra-specifc and inter-specifc 29 30 mainland Southeast Asia, showed high negative resid- levels (Abolins et al. 2011; Tian et al. 2015), indicating 30 31 ual values of allelic diversity, supporting the prediction further need for eco-immunological studies in the natu- 31 32 of a loss of immunogenetic diversity following its inva- ral environment, including both native and invaded hab- 32 33 sion in mainland Southeast Asia. However, there are no itats. All empirical studies on the immunocompetence of 33 34 available data to test the corollaries of these predictions invasive species so far have been done on bird and am- 34 35 as R. exulans and R. tanezumi were not screened for phibian species (e.g. Martin et al. 2010; Brown et al. 35 36 MHC outside mainland Southeast Asia. 2015). The immunocompetence of invasive species may 36 37 Moreover, as half of the genetic variability conferring have consequences for spillover. Using a mathemati- 37 38 resistance against parasites and pathogens is attribut- cal approach taking into account historical data from a 38 39 able to non-MHC genes, further immunogenetic studies plague outbreak that occurred in Saxony in 1614–1615, 39 40 of invasive Rattus should also include these (e.g. Toll- Monecke et al. (2009) conclude that the spread of R. 40 41 like receptors) and not only the MHC (Acevedo-White- norvegicus might have contributed to the disappearance 41 42 house & Cunningham 2006). Fornůsková et al. (2013) of Black Death epidemics from Europe in the 18th cen- 42 43 sequence the genes encoding Toll-like receptor 4 (Tlr4) tury. This would have occurred through the competitive 43 44 and 7 (Tlr7) across several species within the subfam- advantage of R. norvegicus over R. rattus in large cities 44 45 ily Murinae from Southeast Asia, including R. tanezu- and due to its immunoresistance to Yersinia species. 45 46 mi and R. exulans. Their results suggest the existence of 46 47 parasite-mediated selection that has shaped the present DISCUSSION: RESEARCH NEEDED 47 48 species-specifc variability in these rodents. 48 Our review supports several non-mutually exclusive 49 The immunogenetic studies should be accompanied 49 hypotheses related to the importance of parasites in the 50 by the characterization of the protective immune phe- 50 success and outcomes of invasion by the major invasive 51 51

1 Rattus species. However, this review also highlights a ease spread should be higher in human dominated hab- 1 2 lack of knowledge, and emphasizes areas of research re- itat due to the synanthropic behavior of these invasive 2 3 quiring investigation. rodents. 3 4 First, there are few studies on co-phylogeography 4 5 of invasive rodents and their associated invasive para- CONCLUSION 5 6 sites. Directly transmitted and specifc parasites should 6 7 be chosen (Nieberding et al. 2004; Nieberding & Oliv- Currently, trade routes are dramatically expanding 7 8 ieri 2007). Co-phylogeographic structures would help to as a consequence of ongoing global economic devel- 8 9 map the historical distribution and invasion routes of ro- opment. The economic rise of Asia and Southeast Asia, 9 10 dents and their communities of parasites. and their importance in global trade are facilitating the 10 11 high risk of new invasions by these four invasive rats. 11 Second, investigations of parasite (macro and micro) 12 Changes in habitat worldwide may also favor the spread 12 diversity in original distributions and invaded locali- 13 of these invasive rodents, especially in insular Southeast 13 ties (historical and recent) using molecular techniques 14 Asia, Melanesia, South America and Africa. The antic- 14 should further help identify co-invasive parasites from 15 ipated resulting climate change is regarded as an im- 15 spillback of local parasites. 16 portant challenge due to its major public health impli- 16 17 Third, measurements of immunological parameters, cations. The effects of climate change on the ecology of 17 18 immune gene diversity and immunocompetence of in- rodents and rodent-borne diseases deserve further atten- 18 19 vading and resident hosts are almost completely lacking. tion. Thus, addressing the above mentioned issues is of 19 A prediction is that immunocompetence and immune 20 high importance, with implications for public health, the 20 genes diversity should be higher in the original species 21 economy and conservation. 21 distribution, especially the costly branches of immuni- 22 22 ty (e.g. infammatory immune responses; Lee & Klasing 23 ACKNOWLEDGMENTS 23 2004). Furthermore, the immunocompetence and im- 24 24 mune genetic diversity should be higher than in non-in- We are grateful for grants received through the 25 25 vasive congeneric species in both original and invaded French ANR Biodiversity CERoPath project (grant 26 26 localities (if present). ANR 07 BDIV 012; “Community Ecology of Rodents 27 27 and their Pathogens in a Changing Environment” [www. 28 Fourth, as the immunocompetence should be linked 28 ceropath.org]) and the French ANR CP&ES Biodi- 29 to parasite diversity (Ponlet et al. 2011), trade-offs be- 29 vHealthSEA project (grant ANR 11 CPEL 002; Local 30 tween levels of immunocompetence and expensive life 30 impacts and perceptions of global changes: Biodiversi- 31 history traits are expected (Bordes et al. 2011; Morand 31 ty, health and zoonoses in Southeast Asia). We thank 3 32 2015) as well as decreased immunocompetence with the 32 anonymous referees for helpful comments. 33 loss of parasites and lower local biodiversity (Møller & 33 34 Cassey 2004). A re-allocation of resources away from 34 35 costly defenses should be particularly pronounced at the REFERENCES 35 36 wave-front of the invasion during the range expansion 36 stage (White & Perkings 2012). Abdelkrim J, Pascal M, Calmet C, Samadi S (2005). 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