sign in sign up
<<
Home , Hassalstrongylus, Marsupial, Rodent, Shrew opossum

University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln

Scott Gardner Publications & Papers Parasitology, Harold W. Manter Laboratory of

2017

Nematodes Associated with in the Great American Biotic Interchange (GABI)

F. Agustin Jimenez Southern Illinois University Carbondale, [email protected]

Juliana Notarnicola Instituto de Biología Subtropical, [email protected]

Scott Lyell Gardner University of Nebraska - Lincoln, [email protected]

Follow this and additional works at: https://digitalcommons.unl.edu/slg

Part of the Biodiversity Commons, Biology Commons, Ecology and Evolutionary Biology Commons, and the Parasitology Commons

Jimenez, F. Agustin; Notarnicola, Juliana; and Gardner, Scott Lyell, " Associated with Mammals in the Great American Biotic Interchange (GABI)" (2017). Scott Gardner Publications & Papers. 20. https://digitalcommons.unl.edu/slg/20

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Scott Gardner Publications & Papers by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Copyright 2017, the authors. Open access material.

Oecologia Australis 21(1): 1-16, 2017 10.4257/oeco.2017.2101.01

NEMATODES ASSOCIATED WITH MAMMALS IN THE GREAT AMERICAN BIOTIC INTERCHANGE (GABI)

F. Agustín Jiménez1*, Juliana Notarnicola2 & Scott L. Gardner3

1 Southern Illinois University (SIU), Department of Zoology, Laboratory of Parasitology, 1125 Lincoln Drive, Carbondale, IL, USA 62901-6501 2 Instituto de Biología Subtropical (IBS) -CONICET, Bertoni 85 (3370) Puerto Iguazú, Misiones, Argentina 3 University of Nebraska-Lincoln (UNL), University of Nebraska State Museum, The Harold W. Manter Laboratory of Parasitology, 900 N 16th St.,Lincoln NE, USA 68588-0514 E-mails: [email protected], [email protected], [email protected] count: 9717 words.

ABSTRACT The Great American Biotic Interchange (GABI) is a large-scale zoogeographic event that illustrates the exchange and diversification of mammals between North and . This phenomenon was accelerated by the connection of both landmasses during the . Support for this phenomenon includes the extant distribution of xenarthrans, didelphiomorph , hystricognath and cricetine , sciurids and , as well as the distribution of in the stratigraphic record and the coalescence of genotypes. Contrasting with the relatively well-documented role and history of mammals in GABI, the role of their parasites has been largely neglected. As a consequence, the reconstructions of the causes of diversification, extinction and dispersion of groups of mammals during the Pliocene (and ) invoke changes in climate patterns and the role of competitors or predators, yet in most cases the lines of evidence are not direct. We posit that infections with parasites offer a direct form of evidence of the role of interactions among , by considering that the successful establishment of species of parasites in new groups of will result in a net effect on their adaptive . Thus, the current distribution of parasites of the families Aspidoderidae, Nippostrongylidae, Onchocercidae, Oxyuridae, Rictaluriidae and Viannaidae offers evidence that the historical associations of these nematodes and their hosts diverge from the expected cospeciation and codivergence. Thus, of parasites infect disparate clades of mammals and, by deviating from the expected cospeciation, represent a paradox. This paradox deters investigators from studying historical associations among symbionts, since researchers lose the compelling simplicity of testing coevolutionary associations through the congruence of their resulting phylogenies. However, the reconstruction of historical associations must acknowledge the differential survival of parasites in novel hosts. This consideration is part of the Stockholm Paradigm, which includes the hypotheses known as Ecological Fitting, Oscillations, Pulses and Mosaics of Geographic Coevolution. We introduce nine host-parasite systems that provide insights on the role of parasites in GABI. We posit that the conservatism of parasite resource use, heritability of the adaptive immune system, and the genetic structure of parasites make it possible to elucidate the role of these parasites in GABI. Keywords: co-evolution; diversification; extinction; historical associations; neotropics.

INTRODUCTION in combination with the study of the rich record throughout North and South America, has enabled The Great American Biotic Interchange biologists to document the net effects of GABI on (hereafter GABI) is the asymmetric swapping of mammalian dispersion, diversification and extinction terrestrial biotas between North and South America (Webb 1978, Simpson 1980, Borrero 2008). In (Webb 1978, Simpson 1980, Stehli & Webb 1985, particular, scientists have estimated dates of the Carrillo et al. 2015; Cione et al. 2015). GABI was impressive adaptive diversification of South American consolidated by the closure of the Panamanian land (Parada et al. 2013, Leite et al. 2014); bridge, which facilitated the flux of organisms identified signals of mass extinction in Didelphiomorpha otherwise restricted to their original landmasses (Webb in the Miocene (Jansa et al. 2014); studied the 1978, Simpson 1980, Marshall 1985, O'Dea et al. 2016). expansion of South American species into The study of extant diversity and distribution, (Arteaga et al. 2012, Feng et al. 2016); 2 Jiménez et al. tested the role of climate fluctuations on diversification or fossilized feces (Araújo et al. 1989, Sardella & of xenarthrans during the (Delsuc et al. Fugassa 2009b, Sardella & Fugassa 2009a, Beltrame 2004), and estimated dates of mass extinction for the et al. 2010; Beltrame et al. 2013). These have endemic South American (MacFadden a greater chance of preservation due to the protective 2006, Prado et al. 2015). In each of these examples of the -shell and their inclusion in the fecal either some sort of biological interaction (i.e., ) matter. Nevertheless, ectoparasites offer a different or a link to a physical change is invoked to explain the outcome in that there are sporadic findings of evolutionary outcome. Among the latter, the organisms attached to the remains of mummified reconstruction of the paleoenvironments supports the wildlife (Dittmar 2000), or traces of infection on dried establishment of links between drastic changes in skins or osteoderms (Hammond et al. 2014 Tomassini climate, on one hand, and patterns of diversification et al. 2016). and extinction, on the other. The establishment of these The pervasive lack of direct fossil evidence has links is made possible by using a time-calibrated hindered the investigations of the evolutionary phylogeny that makes it possible to test the likelihood associations between parasites and mammals. This is of association of said events with internal nodes of the because the lack of material evidence impedes both phylogeny. However, the case of biological interactions the unequivocal diagnosis and taxonomic assignation relies more on extrapolation of the present interaction of a parasite into a taxonomic group and the among associates and to some degree on their establishment of the association among ancestral phylogenetic conservatism. As such, most mammals parasites and their ancestral hosts. Both of these are of the will be construed as predators necessary because a precise taxonomic assignation of small mammals. In the case of GABI, predation by and identification of a geological context facilitate the more efficient carnivores and competition (or lack establishment of minimum ages of the association and thereof) are the most commonly invoked interactions are a prerequisite for calibration of a that determine the fate of certain mammal groups used for phylogenetic reconstructions. Nevertheless, (Jansa et al. 2014). Yet, the role of parasites and determination of both the origin of host-parasite parasitism as a significant biological interaction is associations is possible by using indirect methods, seldom considered as an important evolutionary force which include the increase of taxon and geographic that shaped GABI. sampling and the calibration of molecular clocks Evidence of infection with micro- and enforcing switches in geographic distribution or macroparasites in extinct mammals and other association with hosts. With the use of ancillary vertebrates, although scarce, is available (Hugot et al. geological evidence, it is possible to estimate the age 2014, De Baets & Littlewood 2015, Poinar 2015). The of associations, especially in those cases that involve scarcity of evidence is in part the result of the low an evident shift in the geographic distribution that is chances of fossilization of the of parasites; after linked to a dated geological event (Ricklefs & Outlaw all, most microparasites are systemic tissue-dwelling 2010, Badets et al. 2011, Outlaw &Ricklefs 2011). unicellular organisms (i.e., they infect cells), thus they Thus, as in other organisms, the study of the evolution would replicate inside soft tissues that decay after of parasites is possible through the analysis of their death. Furthermore, their pathological effects on the genetic structure (De Baets & Littlewood 2015), hosts are mostly evident in these same tissues and which again can be dated by correlating shifts in the seldom evident on the skeletal system, which has a distribution of parasites in their hosts or in new greater chance of fossilizing. Internal macroparasites geographic areas. are no different in that these infect the intestine and The study of the diversification of parasites as other visceral organs that have low chances of a result of episodic geological/climatic changes, such fossilization. As a consequence, most of the evidence as the closure of the Panamanian isthmus, is relevant of the presence of parasites in Holocenic vertebrates because it makes it possible to establish the causality consists of eggs of these parasites present in coprolites of these sudden changes in several ways, including: a)

Oecol. Aust., 21(1): 1-16, 2017 The Nematodes Associated with Mammals in GABI 3 the current distribution of species, b) rates of species resources by evading or overcoming the immune extinction, c) establishment and dispersion of invasive response presented by their hosts and by becoming species, and d) exchange or transfer of established in their specific site, in which they will have among the faunal elements involved (Ricklefs & the chance to either undergo or Outlaw 2010, De Baets & Littlewood 2015, Poinar experience growth via asexual amplification. 2015). Information derived from these phenomena may help in better understanding the consequences of the What is a host? establishment and rapid dispersion of ecological invaders, which in the present time may result in the The host is the individual organism that harbors spread of novel emerging diseases that threaten wildlife the parasite and it features phenotypic traits that make and the human population (Brooks et al. 2014, Hoberg the establishment, survival, and reproduction of the et al. 2015, Hoberg &Brooks 2015). The integration parasite possible. The host contains all of the resources of ecological, micro- and macroevolutionary that facilitate the survival, growth and reproduction of phenomena offers an optimal framework in which to the parasite; thus, both (host and parasite) are said to reconstruct the effects of dispersal, cospeciation, host- be compatible (Combes 1991). This compatibility, when switching and diversification of parasites into new considered from the perspective of the host organism, hosts (Hoberg & Brooks 2015). includes an innate and an adaptive immune system. In this review, we identify the background The immune system of vertebrates includes antibodies information that may facilitate the study of parasites encoded by genes or gene families that may or may in this intercontinental exchange; we introduce case not be exaptations to a parasite or group of parasites. studies that account for the identification of clades with These genes are responsible for initially coding the members in both land masses; we identify clades of immune system to recognize the parasites that are parasites that switched among groups of mammals invading an individual host and for subsequent involved in GABI, and we identify the future directions elaboration of the immune response against the in the research aimed at understanding the role of variously invading parasitic or infective agents. Other parasites in GABI. We posit that there are sufficient elements of the phenotype of organisms, such as elements to act as the foundation for investigating the behavior and physiological traits increase their chances role of parasites in GABI. of encountering parasites and facilitate infection (Combes 1991). These phenotypic elements are likely What are parasites? inherited from a common ancestor, yet in some cases they may be the result of evolutionary convergence. Parasitism is a symbiosis, a biological interaction among members of different taxa, in which the parasite Distribution of parasites in vertebrates will consume parts or the totality of the infected individual, the host. Parasitism has arisen independently In natural conditions, parasites will form large in 223 lineages (Weinstein & Kuris 2016). Most populations by concentrating several individuals in only of these events are concentrated among three phyla - a few hosts. These aggregations are in fact populations Arthropoda, Nematoda and Platyhelminthes- which that feature their own dynamics (Nadler 1995). show a relatively successful diversification and Generally, each of these populations concentrates association with vertebrates (Poulin & Morand 2000, sexual individuals, and their consolidation or grouping Weinstein & Kuris 2016). In general, parasites are is regulated by biotic and abiotic factors that determine specialized consumers of resources available in their their mode and efficiency of transmission (Pavlovsky hosts, and as such they feature phylogenetic 1966). As a consequence, a cluster of populations may conservatism towards these resources and exhibit concentrate in areas that facilitate this transmission pronounced site specificity (Janz et al. 2006; Agosta and this may not correspond with the entire distribution et al. 2010). Parasites must gain access to these of the animal population that can serve as hosts.

Oecol. Aust., 21(1): 1-16, 2017 4 Jiménez et al.

Whereas the immediate effects of the parasite are in would result in the extreme specialization of parasites their host (i.e., pathology), the evolutionary and a narrow host spectrum (de Vienne et al. 2013). consequences of parasites in populations of vertebrates If cospeciation was the driving force of parasite occur downstream through time and space; selection diversification, one would expect that all mammals in is occurring at the level of the individual but it is a would be infected by parasites that are manifested by changes in gene frequencies through phylogenetically related, which is seldom the case time in the host population (Anderson & May 1982, (Light & Hafner 2008). The expectation of May & Anderson 1983). These associations are the encountering mirroring or concordant phylogenies is result of the interactions among the parasites and the based on two premises: (1) that species of permanent elements of the adaptive immune system of vertebrates, parasites are extremely host-specific, specializing in which can be identified in the hypervariable regions of resources exclusively available on their host species; the Major Histocompatibility Complex II, which and (2) that parasites are able to transmit among encodes for antibodies that bind antigens presented by potential hosts via contact and they are able to complete parasites. The signal for these associations has been their life cycle without leaving the host body. As a identified in several groups of small mammals across consequence, these parasites would be a proxy of the South America (Meyer-Lucht et al. 2008, Meyer- phenotype of the host; thus the reconstruction of the Lucht et al. 2010) relationships of these hosts necessitated the inclusion of parasites as an additional character (Fahrenholz Parasites may successfully infect several species 1913, Kellogg 1913). In spite of its circular reasoning of vertebrates (Klassen 1992, de Vienne et al. 2013), and the fact that most parasites are not permanent in or on their The phylogenetic conservatism of permanent hosts, these premises have prevailed in the scientific parasites towards their resources has been considered literature up to the current time. The expectation of as evidence of their pronounced taxonomic specificity maximum cospeciation is not congruent with the towards their host (Fahrenholz 1913). However, this restricted geographic distribution of several parasites. generalization seldom holds when one considers For example, to explain the distribution of parasites that feature one or more free-living stages japonicum, a trematode parasite that infects , (Euzet & Combes 1980, Agosta et al. 2010). In natural rodents, artiodactyls, perissodactyls and carnivores, one conditions, the infective free-living stages are exposed would need to explain their extinction in the rest of to a myriad of potential hosts. The phenotype of the mammalian lineages, including those present in the vast majority of these would be incompatible with the same geographic area (i.e., pholidont ). Both parasite and make the establishment of the parasite resource specialization and the restricted geographic impossible. However, phylogenetically related distribution of clades of parasites combined with their organisms may offer the same resources and ability to infect other hosts and diversify constitute compatibility to parasites (Agosta et al. 2010). the “parasite paradox”. This also suggests that the Furthermore, non-related organisms may also offer narrow geographic distribution of most parasite similar resources and compatibility to parasites, species is an artifact of a limited sampling (Agosta et provided these organisms feature convergent al. 2010). After all, most species of parasites are behavioral or physiological characteristics (Janzen known only from the original description, and 1985, Agosta et al. 2010, Nylin et al. 2014). extensive surveys of parasites have demonstrated that a species of parasite may be able to infect, grow and Historical associations: Does cospeciation explain reproduce in several species of competent hosts the distribution of all parasites? (Notarnicola et al. 2010, Notarnicola et al. 2012). Cospeciation between parasites and their hosts, as in Parasite diversification cannot be explained other symbionts, are expected to occur in nature; based on the process of strict cospeciation, since this however, convincing cases that explain the

Oecol. Aust., 21(1): 1-16, 2017 The Nematodes Associated with Mammals in GABI 5 diversification of entire clades of parasites are rare be geographical, that is through space and time; thus, (de Vienne et al. 2013). the host-parasite associations may be modified by abiotic changes that affect the associations in Independent events in parasites: The stockholm punctuated geographic space. paradigm The Stockholm Paradigm has not yet been widely accepted as a universal framework that helps The success of parasites as exploiters of to explain the origin of host-parasite associations. This reproducing resources (progeny of their host) can be is partly because the Stockholm Paradigm includes at explained by the interplay of four phenomena, which least four different hypotheses, each with its own set allow parasites to increase their host range by infecting of predictions that must be tested at micro- and new organisms and establishing viable populations in macroevolutionary levels. Consequently, most times them; these populations then become isolated and they require different lines of evidence, including undergo their own population dynamics by becoming observations derived from experimental infections. fragmented. This complex interplay of hosts and Furthermore, several host-parasite systems span parasites through evolutionary time is known as the different groups of over vast areas, and it is Stockholm Paradigm (Hoberg et al. 2015, Hoberg & common that these groups of host animals feature Brooks 2015), and it integrates the concepts of different dynamics. This contrasts with the simplicity Ecological Fitting -ability of apparent specific parasites of the premise of maximum cospeciation, in which the to infect a new host that features the conservative apparent information derived from the host and parasite resource the parasite exploits- (Janzen 1985), the distributions, interactions and demographics seems to Oscillation hypothesis - consolidation of new host- suffice to provide the necessary evidence to test the parasite associations though the expansion of the host null hypothesis. range of parasites that enable them to become To this effect, the Stockholm Paradigm is a generalists and give place to specialists- (Nylin et al. holistic approach that promotes the simultaneous study 2014), Taxon Pulses -diversification of a clade of of micro- and macroevolutionary events in a single organisms as a result of the invasion of a new area- host(s)-parasite system, and forces researchers to (Erwin 1981) and the Geographic Mosaic Theory of determine compatible hosts in nature by surveying the Coevolution -persistence of the newly formed presence of parasites, define the nature of the specificity associations through reciprocal adaptations- of a parasite towards its host, characterize the population (Thompson 2005). In conjunction, these phenomena dynamics of the parasite, establish the effect of abiotic explain the distribution of parasites in related and phenomena in the evolutionary history of the parasite unrelated hosts as a consequence of three lineage, and identify putative host-switching events, characteristics of the parasites. These include i) the extinctions and instances of cospeciation. It is possible ability of parasites to use inherent phenotypic plasticity to detect most of these signals from a single dataset, in the characters that enable them to infect a host, ii) yet again this dataset must include information that is evade its immune response, and iii) access and exploit useful at both the micro- and macroevolutionary levels phylogenetically conserved resources present in their (Peter & Slatkin 2013). hosts. Once established into a new species of host, the ancestral population of parasites would experience Parasites in geological history rapid growth or expansion, followed by a subsequent contraction in geographic or host-range. The resulting Evidence of a parasitic lifestyle in forms from fragments of the species or populations would be driven ancient geological areas is scarce; yet, the scientific by the frequency of the host-parasite encounter, community recognizes that extinct animal forms would resulting in microevolutionary dynamics that determine have been infected by parasites (Hugot et al. 2014, the cohesion of a population. It is important to note De Baets & Littlewood 2015, Poinar 2015). The role that the expansion and contraction of the parasites may of pathogens and parasites has been acknowledged

Oecol. Aust., 21(1): 1-16, 2017 6 Jiménez et al. by paleontologists, some of whom invoked the putative mammals, which in addition featured a relatively low role of pathogens in the extinction of the endemic fecundity (many, if not most, Hystricognath rodents, megafauna of South America (Ferigolo 1999). In a marsupials and xenarthrans have a relatively low series of at least 5 conjugations of Biotic Systems intrinsic rate of natural increase relative to the invading (expansions, contraction and switches of pathogens sigmodontine rodents). In summary, the pathogens and their hosts) and Turning Points (abiotic crises or newly arrived in South America posed an episodic events that affected the fauna) spanning from insurmountable challenge to the immune system of the the early to the Holocene, Ferigolo (1999) South American endemics, resulting in their decimation; hypothesizes that the change in faunas may have furthermore, their low fecundity rate and slow growth exposed dispersing animals to different pathogens. This may have resulted in their rapid extinction (Ferigolo mixing, and subsequent exposure resulted in the 1999). The role of pathogens in the extinction of South establishment of parasites in new hosts, thus promoting American megafauna has yet to be evaluated using a host-switch that may have resulted in the extinctions direct or indirect evidence. Although there is a limited of the new hosts through geographic space. number of fossilized parasites and those available Furthermore, the pathogens may have been able to render little information as to the timing of the expand throughout the continent by infecting new diversification of parasite lineages, the framework of organisms from different naïve species as they were episodic or abiotic changes, and the dating of the encountered. extinctions and invasion of mammals are available. This Interestingly, Ferigolo’s hypothesis is in line with would make it possible to test their effect on the the Stockholm Paradigm in that it explains the expansion evolution of parasites, by evaluating for signs of of the geographic range of mammals along with their contraction or expansion in their genetic structure. pathogens/parasites and their ability to infect other In the following, we present an interpretation of endemic South American mammals through Biotic the studies that offer some insight into the role of Systems and Turning Points. In this context, Biotic nematodes in GABI (Summarized in Table 1). We Systems are defined as expansions, contractions and attempt to dissect these studies and address the points switches of pathogens and their hosts, three phenomena they make relative to the Stockholm Paradigm. The that are consistent with Ecological Fitting and goal is to help the reader in identifying the role of these Oscillation; Turning Points consist of abiotic crises or parasite-host model systems in GABI, and in detecting episodic events that affected the fauna, these episodic strengths and weakness of each of the associations events are also consistent with Taxon Pulses in cases studied. Because of their limited taxon sampling, in which the crises enabled the dispersion and geographic distribution or methodology, none of the diversification of taxa in new landmasses. Furthermore, studies addresses all four tenets of the Stockholm Ferigolo’s hypothesis even contemplates the Paradigm. However, with the aid of ancillary Geographic Mosaic Theory of Coevolution, by information, we hope to present a compelling case for acknowledging a long period of coevolution among the merits of the study of parasite-host associations in parasites and mammals in the Northern Hemisphere the study of GABI and to highlight the usefulness of prior to their southward dispersal. This coevolutionary intensive surveys of extant parasites, analyses of their period would have resulted in the acquired immunity distribution, genetic structure and tests of specificity to the current assemblage of Nearctic parasites to understand their impacts in the past events that infecting the mammals dispersing southwards after the determined the current distribution of mammals. continental connection. This phenomenon of coevolution has been amply documented for parasites MATERIAL AND METHODS and mammals in the Northern Hemisphere (Hoberg et al. 2012). The proper information necessary to build The study of parasites involved in GABI includes or to develop the adaptive immunity was not manuscripts documenting the empirical evidence for widespread in the South American Neotropical the presence of fossilized parasites; systematic

Oecol. Aust., 21(1): 1-16, 2017 The Nematodes Associated with Mammals in GABI 7 appraisals of parasite taxa associated with mammalian biogeographical patterns and historical associations taxa involved in GABI; and the reconstruction of with mammals through the phylogeny of the parasites.

BOX 1. The continuous evolution of nematodes of mammals in the New World is shaped by the geological events that bridged the North and South American landmasses. The reconstruction of the phylogeny of parasites and the mapping of their hosts reveal their ability to infect distantly related mammals that converge in habitat (gray rectangles).These interactions are shaped by biotic (mammal cladogenesis) and episodic events (Formation of the Panamanian Land Bridge): At present time 0, populations of parasites appear to be isolated in newly arrived mammals and diverge significantly one from the other by isolation. In -1, the closure of the Panamanian Land Bridge (episodic event) consolidated the exchange and flux of biotic elements between both landmasses. This event included the southward invasion and diversification of several groups of mammals originally from North America (Taxon Pulses of cricetid and geomyid rodents). The Ecological Fitting of local parasites enabled them to infect these newly arrived mammals. In -2, parasites from the group involved in host switching act as generalists and infect organisms from a disparate group of mammals; these parasites may become isolated in the newly acquired host, form a population and diverge genetically from the original population (Oscillation Hypothesis), thus completing a new event of host switching. In -3, the phylogeny of a fictional group of parasites is contrasted against the phylogeny of a group of mammals, events such as host switching, cospeciation, duplication and extinction are illustrated for the parasites (modified from Paterson & Gray 1997).

Oecol. Aust., 21(1): 1-16, 2017 8 Jiménez et al.

PARASITES IN GABI Biogeographical interpretation of systematic appraisals Direct evidence of parasites in ancient times: Eggs in coprolites In the tradition of the study, description and characterization of monophyletic groups, several In the first place, the empirical studies chiefly systematists have hypothesized the origin of certain examine coprolites, which are the fossilized fecal families of parasites in taxonomic monographs. Among matter, of cricetid or hystricognath rodents and enable the lineages of nematodes that appear to be associated the detection of parasite eggs (Araújo et al. 1989, with cricetid rodents, three were used to formulate Sardella &Fugassa 2009b, Beltrame et al. 2010, reconstructions of their biogeographic origin. These Beltrame et al. 2013, Beltrame et al. 2016). In most include nematodes of the Helligmonellidae, Spiruridae cases, evidence of parasites consists of only eggs or and Syphaciinae (Quentin 1969, Quentin 1971, Durette- remains of eggs, which hinders the identification of Desset 1985, Hugot 1988). Species of these taxa are parasites to a species level. This is due to their associated with cricetid rodents, which are an important degraded nature, morphological conservatism and the faunal element of GABI, in that they apparently invaded fact that most characters with which species-level South America from North America once, and their identifications can be made are located in the body diversification into approximately 400 species of the adult; thus, identification is possible only to the accelerated since the Miocene (Parada et al. 2013). family level. When it is possible to make identifications The taxonomic decisions and interpretation of the to the species-level from eggs only, the identification evolutionary relationships of , Spiruridae of species is largely based on the presence of a known and pinworms of the subfamily Syphaciinae (Quentin species of parasite infecting the same host in the same 1969, Quentin 1971, Durette-Desset 1985, Hugot 1988), or closely related areas (Araújo et al. 1989; Sardella was influenced by their putative specificity to their hosts, & Fugassa 2009a); however, this may vary depending most of which were known only from their original on the level of uniqueness of the parasite host description. Based on the analysis of the putative sister association (Hugot et al. 2014). The identification to clades available to the authors, these parasites were the species level of the parasite eggs in related hosts postulated to be host-specific and their origin was presupposes the specificity of the parasite and hypothesized to be in North America. assumes that coprolites from the Holocene do belong Nevertheless, instances of putative host switching to the same species as those we detect in the present were identified in the study of Pterygodermatites, a day. Available studies to date provide records for group of intestinal spirurioid nematodes with a life-cycle parasites of different lineages across the continent, that definitively requires the involvement of an and evidence of range contraction of some species invertebrate intermediate host (Quentin 1969). Species of parasites. For example, the nematode of this genus can be allocated to at least three lineages, Paraspidodera uncinata, is a common parasite of recognized as subgenera, the of each extant hystricognath rodents in Argentina, with the supported by the configuration of the buccal capsule documented southernmost edge of their extant and orientation of their stoma along with the peculiar distribution located in the southern end of Buenos arrangement of body spines (Quentin 1969), which are Aires province (Rossin et al. 2004). Eggs of this rather rare in nematodes. In particular, species of species have been detected in coprolites from Pterygodermatites (Paucipectines) have been , 1,480 km from the nearest known extant recorded from , cricetid rodents, sciurids, didelphid locality for this species (Sardella & Fugassa 2009a). marsupials and xenarthrans (Quentin 1969, Navone 1987, This finding would suggest that the species expanded Jiménez &Patterson 2012). According to the hypothesis southward some time in the past and experienced a of Quentin, two lineages within this clade spread through population contraction that resulted in its Siberia and North America, with the species in North disappearance from present day Patagonia. America subsequently dispersing into South America

Oecol. Aust., 21(1): 1-16, 2017 The Nematodes Associated with Mammals in GABI 9 with their cricetid hosts and then undergoing a of host-parasite associations. Which were documented host-switch -dubbed “host capture” or phénomène du based on the sporadic encounter of a population of capture- by both marsupials and bats (Quentin 1969). parasites in a single individual host. A similar pattern was described for trichostrongylid nematodes in Helligmonellidae, and it Experimental tests of host specificity occurs in species of the Nippostrongylinae (Durette- Desset 1985), nematodes of direct life cycle that infect Since most of the species of parasites that infect their host via skin penetration. In this case, the lineage of mammals of GABI are known from the original the cricetid-dwelling Nippostrongylinae would have description, the evidence for their host specificity -the originated with rodents dispersing from Asia into North number of species of vertebrates infected by a given America, and these subsequently dispersed into South parasite- is rare. In several instances, surveys of mammal America with their cricetid hosts. In contrast, Durette- fauna in defined regions facilitate the detection of Desset (1985) identifies that at least two lineages of frequency of the association of a species of parasite with trichostrongylid nematodes, the Anoplostrongylinae and one or more species of mammals (Guerrero 1985, Kinsella Viannaiidae, may have originated in South America and 1991, Navone et al. 2009, Notarnicola et al. 2010, Simões moved northward. In the case of Anoplostrongylinae these et al. 2010, Solórzano-García et al. 2016). Yet, nematodes would have dispersed with bats and , experimental evidence of the host specificity of these and in the case of Viannaiidae their dispersion would be parasites is scarce; most of the empirical evidence derives linked to didelphid marsupials. Nevertheless, the northward from the study of the low host-specificity of rodent- dispersion of species of Viannaiidae resulted in the dwelling species of Litomosoides, which rely on some presence of three extant species in mammals north of species of arthropod as a vector (Bain et al. 1989, Bain the , which presents a stark contrast &Philipp 1991). Experiments on the specificity of the to the presence of over 60 named species of adults demonstrate that microfilaria of this vector borne Nippostrongylinae present in South America (Durette- nematode can cause infections on rodents of several Desset 1985). This is consistent with the asymmetric unrelated lineages, and that in some cases, the immune distribution of the mammal fauna associated with GABI. response of these rodents needs to be challenged so the Lastly, in the systematic appraisal of the adults become established (Hawking & Burroughs 1946, Syphacinae, Hugot (1988) highlighted the close affinity Pringle & King 1968, Dhar & Singha 1971, Siddiqui & of members of Syphacia towards their hosts that consist Kershaw 1976, Babayan et al. 2003). Their low specificity of both arvicoline and cricetid rodents. These nematodes has been used to investigate the ability of the nematodes feature a direct life cycle and infection is attained through to circumvent the immune system of their novel hosts the ingestion of the eggs. Here again, the putative (Pringle & King 1968). pronounced specificity of these pinworms towards their hosts and the current distribution of extant species in The reconstruction of ancestral states using the New World were used as an argument to postulate statistical tests the origin of this genus in the Palearctic, dispersion towards North America, and subsequent dispersion into Species in the genus Litomosoides are distributed South America. from southern Mexico to northern Patagonia in Argentina Unfortunately, none of these three hypotheses and Chile, totaling 42 species parasitizing didelphiomorph presented above were produced using a phylogenetic marsupials, bats, sciurids, hystricomorph and myomorph framework that allowed testing ancestor/descendant rodents (Notarnicola et al. 2010). Apparently, the relationships by means of a test of ancestral character ancestor of this clade originated in bats from South reconstruction. Furthermore, there is little or no America and they switched to cricetid rodents when information relative to the geographic distribution and these dispersed into the continent roughly 5 mya host associations of most species of parasites. Thus, according to the estimate by Bain and Philipp (1991). the interpretations were based largely on the frequency This group of nematodes shows frequent host-switching

Oecol. Aust., 21(1): 1-16, 2017 10 Jiménez et al. and invasions of mammals of different lineages, including clade that includes parasites that switched from armadillos hystricognath rodents and didelphiomorph marsupials. to cricetid rodents and didelphiomorph marsupials; and a The group was studied using a phylogenetic analysis of second clade that includes parasites that switched from morphological characters that resulted in a non-resolved armadillos to hystricognaths and then to geomyid rodents. phylogeny (Brant & Gardner 2000). Using this The same analysis reveals that at least five lineages of , the authors did not find support for the parasites crossed northward the Central American hypothesis of an origin in bats, but in their reconstruction, isthmus independently. These results are consistent with the topology was consistent with the origin of the group the expectations of a clade of parasites in which the in the area of South America. descendants demonstrate phenotypic plasticity to use Furthermore, in an analysis of the morphological resources available in different hosts, as well as the ability traits derived mostly from original descriptions of species, to evade their hosts’ immune response. This enabled Pérez-Ponce de León et al. (2000), reconstructed the parasites to increase their host range and to expand their phylogenetic relationships of several species of geographic distribution as their hosts dispersed into new Stilestrongylus, a genus of cricetid-dwelling areas (Box 1). Nippostrongylinae that have a geographic range that There are two studies that concentrate on a fraction includes southern North America, Central and South of species of parasites that infect mammals of GABI. America. The phylogenetic and biogeographic analysis On one hand, the reconstruction of characters for of the species of Stilestrongylus revealed that this genus Viannaiidae, a group of nematodes that occur chiefly in is constituted by two lineages: A) one lineage represented didelphiomorph marsupials and some hystricognath by species of Stilestrongylus distributed in the northern rodents, suggests a South American origin of the Neotropical region west of the , with a range -dwelling parasites and their subsequent extending from central Mexico, south to Colombia, and dispersion into North America (Scheibel et al. 2014). On west of the Andes to Chile, and B) a second lineage the other hand, studies on the genetic structure of species formed by species distributed to the east of the Andes of Trypanoxyuris (pinworms of New World primates) representing the southeastern Neotropical lineage north of the isthmus of Panama, have revealed the (Peìrez-Ponce de Leoìn et al. 2000). This reconstruction presence of at least five species of pinworms occurring reveals that sister-group relationships are better in three species of monkeys (Ateles geoffroyi, Allouata explained by geographic proximity rather than by palliata and Allouata pigra) (Solórzano-García et al. taxonomic affinities with their hosts (Pérez-Ponce de 2015, Solórzano-García et al. 2016). Studies on these León et al. 2000). These results are concordant with two systems show the persistence of groups of parasites the origin and subsequent diversification of cricetid that predated the faunal exchange and have been able to rodents in South America. In addition, new records for disperse northward with varying levels of success in species of Hassalstrongylus and Guerrerostrongylus adaptive diversification. The analyses presented in these appear to contribute to this hypothesis (Digiani et al. studies reveal some level of coevolutionary history 2015; Weirich et al. 2016), in that the majority of the between the parasites and their putative ancestral hosts. species are present in defined of the South Table 1 summarizes 9 host-parasite systems that American continent and the parasites are frequently involve faunal elements of GABI. In this table we identify found in unrelated species of cricetid rodents. 7 systems that relied on datasets that could be expanded Additional phylogenetic reconstructions have relied to include new evidence in the form of taxa or characters. on DNA to infer the relationships among parasites, and Additional taxa from a larger geographic scale may these phylogenies have served to test biogeographic facilitate the test and reconstruction of macroevolutionary scenarios and patterns of historical association (Jiménez- phenomena. Alternatively, incorporation of additional Ruiz et al. 2008; Jiménez et al. 2012; Jiménez et al. characters that facilitate the detection of population 2013). The analysis of the Aspidoderidae led to the expansion or contraction may provide evidence of discovery of two clades that concentrate the events of microevolutionary phenomena, including but not limited host switching. In the first place, there is a South American to ecological fitting, oscillations and taxon pulses.

Oecol. Aust., 21(1): 1-16, 2017 The Nematodes Associated with Mammals in GABI 11 Evidence of of Evidence Taxon Pulse Pulse Taxon NO NO Mosaic of Mosaic Evolution Geographic formation available for a particular a for available formation rgence of specialists from generalists) from specialists of rgence NO NO NO NO NO NO NO NO NO YES YES NO NO radigm. Ecological Fitting (ecological 1946) 1946) Burroughs Burroughs Oscillation Hawking & Evidence of (available in (available ge) are macroevolutionary phenomena. macroevolutionary are ge) et . l associations involves increase of host-range and host-range of increase involves associations l . et al et . 2011; . 2011; 2011) 2011) etal . 2011) . 2011) . 2013) . 2013) et al et et al et al. et al Evidence of . 2012) 2012) . EcologicalFitting Kinsella 1991) Notarnicola 2010;Simões 2011; Notarnicola al Simões Simões Jiménez Byles Explicit test of of test Explicit historical associations biogeographicaffinity / NO NO NO NO NO NO data YES YES YES (available in YES YES YES YES YES YES NO YES (available in YES YES (available in NO YES YES YES YES YES YES NO to include new new include to Methods allow Methods . . et et al et et al et . 2000) 2000) . et et al et . 2015; 2015; . 2014) . 2016) 2016) . Macroevolution Macroevolution Reconstruction of of Reconstruction (Quentin 1969) (Brant & Gardner 2000) NO NO YES (available in (Hugot 1988) et al YES Solórzano-García al 1985) NOLeón (Scheibel al. YES (available in (Jiménez-Ruiz 2008; Jiménez 2012) (Gardner 1991) YES YES NO NO YES YES in the New World Cricetid rodents, bats, bats, rodents, Cricetid didelphiomorph sciurids, marsupials sciurids, bats, rodents, didelphiomorph marsupials rodents Monkeys World New Monkeys World New 1999) (Hugot (Solórzano-García rodents Cricetid YES rodents Cricetid Didelphiomorph (Durette-Desset marsupials, Hystricognath rodents de (Pérez-Ponce YES NO NO NO YES Hystrocognath and and Hystrocognath rodents, cricetid didelphiomorph marsupials, geomyids and Hystricognath Geomyid rodents Hystricomorph rodents (Hugot 2003) YES YES NO NONO NO NO NO NONO YES YES 2003) (Hugot rodents Hystricomorph Geomyid and cricetid cricetid and Geomyid

. Summary of historical associations among mammals involved in GABI and their parasites. The columns represent a summary of in of summary a represent columns The parasites. their and GABI in involved mammals among associations historical of Summary . Group parasitesof Recorded hosts Spirurata Spirurata Pterygodermatites Litomosoides Oxyurida Syphacinae Helminthoxys Trypanoxyuris cricetid and Arvicoline Trypanoxyuris Trichostrongyloidea Nippostrongylinae Stilestrongylus Viannaiidae Heterakoidea Aspidoderidae Armadillos, Paraspidodera

Table1 mammal - parasite system, which may allow the reconstruction of ecologica the evolution (interspecific of Oscillation these associations and as part capabilities) of host-use the Stockholm novel Pa of evolution prior without hosts other infect specialists (eme Evolution of Mosaic Geographic the speciation, involve they Because phenomena. microevolutionary are isolation) subsequent chan episodic an to due isolation and expansion biotic of episodes alternating from results diversity (species Pulses Taxon and

Oecol. Aust., 21(1): 1-16, 2017 12 Jiménez et al.

DISCUSSION The case of Aspidoderidae provides different tests on the micro- and macroevolutionary phenomena Future directions that have shaped this association. First, the association of Paraspidodera uncinata and Ctenomys spp. in The case of species of Pterygodermatites is Bolivia offers evidence of a very localized Geographic interesting, since some species of this genus are known Mosaic of Coevolution. This is concordant with the to occur in a variety of mammals (P. p e ro m y s c i is geographic isolation of each of the populations included present in different species of and in the study (Gardner 1991). Second, there is evidence Neotoma; P. elegans in bats and marsupials). of the dispersion of these parasites from South into However, there is no comprehensive analysis of the North America, and evidence of host switches that distribution of the several species present in South are a result of the Taxon Pulses combined with America, which is a necessary prerequisite to Oscillations suffered by these worms. Nevertheless, understand the role of Ecological Fitting and this evidence is not supported by exhaustive sampling Oscillations in the consolidation of any association. of the genetic structure of members of closely related In the case of Syphacinae (pinworms), some populations. This evidence awaits to be produced and studies have documented that a single species is able tested in the proper theoretical framework. to infect several species of rodents. This is consistent Moreover, the recent description of the with Ecological Fitting and has been documented in geographic and genetic structure of four species of both North and South America (Kinsella 1991, Simões pinworms in two different species of New World et al. 2011). However, observations derived from monkeys offers evidence of a Taxon Pulse, and surveys of akodontine rodents in Argentina suggest Oscillation. This is mainly because the system that this phenomenon is not universal, because it originated in South America but the evidence used in appears that species-specific pinworms are present the study is present north of the Central American throughout the South Cone (Robles, 2010). Similarly, isthmus. the members of Nippostrongylinae appear to show high Finally, the presence of preserved eggs of host-specificity. Nevertheless, Oscillations and parasites in coprolites highlights the notion of sustained Ecological Fitting are documented for several species infections throughout geological time. One may argue in the eastern portion of South America (Simões et al. that the vast majority of these records belong to a recent 2011, Simões et al. 2012, Digiani & Durette-Desset age (Holocene); however these records assist in 2014). The use of genetic markers may perhaps shed detecting variations in the distribution of the parasites some light on the distribution of a single lineage of and their association with particular groups of rodents parasites in several species of rodents. (Sardella & Fugassa 2009a). In the case of vector-transmitted parasites, five The study of the genetic structure of parasites of the 27 species of Litomosoides parasitizing rodents makes it possible to elucidate the role of parasites in and marsupials and three of the 15 species parasitizing GABI, not only as a proxy of diversification, but also bats appear to exhibit low host-specificity, e.g. L. as evidence of a variety of infective agents that brasiliensis is recorded from six host species, L. challenge the hypervariable regions of the adaptive navonae in five host species, L. pardinasi in four immune system. To this effect, the interaction between host species (including sp.), L. hoplomys, L. these hypervariable regions and the parasite diversity sigmodontis, L. chandleri and L. hamletti in two is yet to be shown in these systems. We recommend a host species each (Notarnicola et al. 2010, Simões parasite-centered approach, in which the genetic et al. 2011, Notarnicola et al. 2012). The detection structure of the parasite is framed on its own of Oscillations should be possible in this group, geographic distribution and biotic associations. This especially because it is made up of clades that feature evidence should be analyzed for the proper signs of putative high host-specificity and clades that exhibit population expansion and contraction that suggest low host-specificity. switches in distribution and biotic interactions (in this

Oecol. Aust., 21(1): 1-16, 2017 7KH1HPDWRGHV$VVRFLDWHGZLWK0DPPDOVLQ*$%,

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tD0DGULG++5DF]6 FDQEHJHQHUDOLVWVUHVROYLQJWKH³SDUDVLWHSDUDGR[´DQG ( 'XUVDKLQKDQ$7)LQGLQJWKHPEHIRUHWKH\ILQG LPSOLFDWLRQVIRUHPHUJLQJLQIHFWLRXVGLVHDVH=RRORJLD   XVLQIRUPDWLFVSDUDVLWHVDQGHQYLURQPHQWVLQDFFHOHUDWLQJ '2, FOLPDWHFKDQJH&RPSDUDWLYH3DUDVLWRORJ\   $QGHUVRQ50 0D\50&RHYROXWLRQRIKRVWVDQG %\OHV%&DW]HIOLV)6FKHLEHO53 -LPpQH])$ SDUDVLWHV3DUDVLWRORJ\   *DVWURLQWHVWLQDOKHOPLQWKVRIWZRVSHFLHVRIPRXVHRSRVVXPV $UD~MR$)HUUHLUD/)&RQIDORQLHUL8&KDPH0 5LEHLUR 0DUPRVD GHPHUDUDH DQG 0DUPRVD PXULQD IURP )UHQFK %6WURQJ\ORLGHVIHUUHLUDL5RGULJXHV9LFHQWHDQG*RPHV *XLDQD&RPSDUDWLYH3DUDVLWRORJ\    1HPDWRGD5KDEGLDVRLGHD LQURGHQWFRSUROLWHV  &DUULOOR-')RUDVLHSL$-DUDPLOOR& 6iQFKH]9LOODJUD 

2HFRO$XVW     14 Jiménez et al.

Fur Tropenmedizin Und Parasitologie, 22(3), 312-325. Philosophical Transactions of the Royal Society B-Biological Digiani, M. C., & Durette-Desset, M. C. 2014. Taxonomic revision Sciences, 370(1665), 20130553.UNSP 20130553. DOI: of the Nippostrongylinae (Nematoda, Heligmonellidae) parasitic 10.1098/rstb.2013.0553 in Oriental . The genus Paraheligmonelloides Fukumoto, Hoberg, E. P., Galbreath, K. E., Cook, J. A., Kutz, S. J., & Pottey, Kamiya & Suzuki, 1980. Zootaxa, 3884(1), 81-88. L. 2012. Northern host-parasite assemblages: history and Digiani, M. C., Notarnicola, J., & Navone, G. T. 2015. Rediscovery biogeography on the borderlands of episodic climate and and new morphological data on two Hassalstrongylus environmental transition. Advances in Parasitology, 79, 1-97. (Nematoda: Heligmonellidae) coparasitic in the marsh DOI: 10.1016/B978-0-12-398457-9.00001-9 chacarius (Rodentia: Cricetidae) from Argentina. Hugot, J.P., Gardner, S. L., Borba, V., Araujo, P., Leles, D., Stock Journal of Parasitology, 101(5), 556-564. DOI: 10.1645/15-746 Da-Rosa, Á. A., Dutra, J., Ferreira, L. F., & Araújo, A. 2014. Dittmar, K. 2000. Evaluation of ectoparasites on the Discovery of a 240 million old nematode parasite egg in mummies of El Yaral and Moquegua valley, in southern Peru. a coprolite sheds light on the early origin of Chungará (Arica), 32(1), 123-125. pinworms in vertebrates. Parasites & Vectors, 7(1), 486-492. Durette-Desset, M. C. 1985. Trichostrongyloid nematodes and DOI: 10.1186/s13071-014-0486-6 their hosts: reconstruction of the phylogeny of a Hugot, J. P. 1988. Les nématodes Syphaciinae parasites de rongeurs parasitic group. Advances in Parasitology, 24, 239-306. et de lagomorphes. Taxonomie, zoogéographie, évolution. Erwin, T. L. 1981. Taxon pulses, vicariance, and dispersal: An Mémoires du Muséum National d’Histoire Naturelle. Série evolutionary synthesis illustrated by carabid . In: Nelson, A. Zoologie, 141, 1-153. G.J.& Rosen, D.E. ( Eds.), Vicariance biogeography : a critique. Hugot, J. P. 1999. Primates and their pinworm parasites: The pp. 159 - 183. New York: Columbia University Press. Cameron hypothesis revisited. Systematic Biology, 48(3), Euzet, L., & Combes, C. 1980. Les problèmes de l’espèce chez 523-546. DOI: 10.1080/106351599260120 les animaux parasites. Mémoires de la Société Zoologique de Hugot, J. P. 2003. New evidence for hystricognath rodent France, 40(3), 239-285. monophyly from the phylogeny of their pinworms. Tangled Fahrenholz, H. 1913. Ectoparasiten und Abstammungslehre Trees: Phylogeny, Cospeciation and Coevolution, pp. 144-173. Zoologischer Anzeiger, 41(8), 371-374. Jansa, S. A., Barker, F. K., & Voss, R. S. 2014. The early Feng, X., Anacleto, T. C. S., & Papes,, M. 2016. Climatic similarity diversification history of didelphid marsupials: a window into of extant and extinct Dasypus armadillos. Journal of South America’s “splendid isolation”. Evolution, 68(3), 684- Mammalian Evolution, 1 - 14. DOI: 10.1007/s10914-016- 695. DOI: 10.1111/evo.12290 9336-y Janz, N., Nylin, S., & Wahlberg, N. 2006. Diversity begets Ferigolo, J. 1999. Late South American land-mammal diversity: host expansions and the diversification of plant- extinctions: The infection hypothesis. In: Rabassa, J.& feeding . BMC Evolutionary Biology, 6.Artn 4. DOI: Salemme, M. (Eds.), of South America and 10.1186/1471-2148-6-4 Antarctic Peninsula, Vol 12 (1996-1997). A balkema Janzen, D. H. 1985. On ecological fitting. Oikos, 45(3), 308-310. publishers, Leiden, Netherlands, pp. 279 - 310. Jiménez, F. A., Carreno, R. A., & Gardner, S. L. 2013. Aspidodera Gardner, S. L. 1991. Phyletic coevolution between subterranean kinsellai n. sp. (Nematoda: Heterakoidea) from nine-banded rodents of the genus Ctenomys (Rodentia: ) armadillos in Middle America with notes on phylogeny and and nematodes of the genus Paraspidodera (Heterakoidea: host-parasite biogeography. Journal of Parasitology, 99(6), Aspidoderidae) in the Neotropics: temporal and evolutionary 1056-1061. implications. Zoological Journal of the Linnean Society, 102, Jiménez, F. A., Gardner, S. L., & Catzeflis, F. 2011. Structure of 169-201. parasite component communities of didelphid marsupials: Guerrero, 1985. Nematoda: Trichosytrongyloidea parasitos de insight from a comparative study. Journal of Parasitology, mamíferos silvestres de .II. Revisión del género 97(5), 779-787. Viannaia Travassos 1914. Memoria de la Sociedad de Ciencias Jiménez, F. A., Gardner, S. L., Navone, G. T., & Ortí, G. 2012. Naturales La Salle, 65(124), 9-47. Four events of host-switching in Aspidoderidae (Nematoda) Hammond, H., Lareschi, M., Zilio, L., Ezquiaga, M. C., & Castro, involve convergent lineages of mammals. Journal of A. 2014. Placas óseas perforadas de Zaedyus pichiy en un Parasitology, 98(6), 1166-1175. contexto arqueológico: ¿elementos confeccionados Jiménez, F. A., & Patterson, B. D. 2012. A new species of antrópicamente o generados por agéntes biológicos? Un Pterygodermatites (Nematoda: Rictulariidae) from the Incan abordaje interdisciplinario. Atek Na, 4, 9-36. , Lestoros inca. Journal of Parasitology, 98(3), Hawking, F., & Burroughs, A. M. 1946. Transmission of 604-607. Litomosoides carinii to mice and . Nature, 158 p. 98. Jiménez-Ruiz, F. A., Gardner, S. L., Noronha, D., & Pinto, R. M. Hoberg, E. P., Agosta, S. J., Boeger, W. A., & Brooks, D .R. 2015. 2008. The systematic position of Lauroiinae Skrjabin and An integrated parasitology: revealing the elephant through Schikhobalova, 1951 (Nemata: Heterakoidea: Aspidoderidae), as tradition and invention. Trends in Parasitology, 31(4), 128- revealed by the analysis of traits used in its diagnosis. Cladistics, 133. DOI: 10.1016/j.pt.2014.11.005 24(4), 459-476. DOI: 10.1111/j.1096-0031.2007.00194.x Hoberg, E. P., & Brooks, D. R. 2015. Evolution in action: climate Kellogg, V. L. 1913. Distribution and species-forming of ecto- change, biodiversity dynamics and emerging infectious disease. parasites. The American Naturalist, 47(555), 129-158.

Oecol. Aust., 21(1): 1-16, 2017 7KH1HPDWRGHV$VVRFLDWHGZLWK0DPPDOVLQ*$%,

.LQVHOOD-0&RPSDULVRQRIKHOPLQWKVRIWKUHHVSHFLHV *( RIPLFH3RGRP\VIORULGDQXV3HURP\VFXVJRVV\SLQXVDQG 1\OLQ66ORYH- -DQ]1+RVWSODQWXWLOL]DWLRQKRVW 3HURP\VFXV SROLRQRWXV IURPVRXWKHUQ )ORULGD &DQDGLDQ UDQJHRVFLOODWLRQVDQGGLYHUVLILFDWLRQLQQ\PSKDOLGEXWWHUIOLHV -RXUQDORI=RRORJ\5HYXH&DQDGLHQQH'H=RRORJLH   $SK\ORJHQHWLFLQYHVWLJDWLRQ(YROXWLRQ  '2, '2,] (YR .ODVVHQ * -  &RHYROXWLRQ  D +LVWRU\ RI WKH 2¶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xDV8)-6DOD]DU%UDYR-'¶(OLD* %LRFKURQRORJ\RIWKH7UDQVDPHULFDQ)DXQDO,QWHUFKDQJH,Q 3DOPD5('DWLQJDQLPSUHVVLYH1HRWURSLFDOUDGLDWLRQ 6WHKOL)* :HEE6' (GV 7KH*UHDW$PHULFDQ%LRWLF PROHFXODUWLPHHVWLPDWHVIRUWKH6LJPRGRQWLQDH 5RGHQWLD ,QWHUFKDQJHSS1HZ

2HFRO$XVW     16 Jiménez et al.

Robles, M. D. 2010. La importancia de los nematodes Syphaciini mamorae (Rodentia: ) in the Pantanal and new (Syphaciinae-Oxyuridae) como marcadores específicos de sus data on the synlophe of Guerrerostrongylus zetta from the hospedadores. Mastozoología Neotropical 17(2), 305-315. Atlantic Forest, Brazil. Journal of Parasitology, 98(4), 801- Quentin, J. C. 1969. Essai de classification des nématodes 805. DOI: 10.1645/Ge-2905.1 rictulaires. Mémoires du Muséum National d’Histoire Simões, R. O., Souza, J. G. R., Maldonado, A., & Luque, J. L. Naturelle, 54(2), 55-115. 2011. Variation in the helminth community structure of three Quentin, J. C. 1971. Sur les modalités d’évolution chez quelques sympatric sigmodontine rodents from the coastal Atlantic lignées d’Helminthes de Rongeurs . Cahiers Forest of Rio de Janeiro, Brazil. Journal of Helminthology, O.R.S.T.O.M., série Entomologie médicale et Parasitologie, 85(2), 171-178. DOI: 10.1017/S0022149X10000398 9(2), 103-176. Simpson, G. G. 1980. Splendid isolation. The curious history of Ricklefs, R. E., & Outlaw, D. C. 2010. A Molecular Clock for South American Mammals., New Haven, MA. Yale University Malaria Parasites. Science, 329(5988), 226-229. DOI: Press: p. 275. 10.1126/science.1188954 Solórzano-García, B., Nadler, S. A., & Pérez-Ponce de León, G. Rossin, M. A., Timi, J. T., & Malizia, A. I. 2004. Redescription 2016. Pinworm diversity in free-ranging howler monkeys and New Host Record of Paraspidodera uncinata (Rudolphi, (Alouatta spp.) in Mexico: Morphological and molecular 1819) (Nematoda, Aspidoderidae) from the South American evidence for two new Trypanoxyuris species (Nematoda: subterranean rodent Ctenomys talarum (Rodentia, Oxyuridae). Parasitology International, 65(5 Pt A), 401-411. ). Acta Parasitologica, 49(4), 325-331. DOI: 10.1016/j.parint.2016.05.016 Sardella, N. H., & Fugassa, M. H. 2009a. Paleoparasitological Solórzano-García, B., Nadler, S. A., & Pérez-Ponce de León, G. analysis of rodent coprolites in holocenic samples from 2015. Trypanoxyuris atelis and T. atelophora (Nematoda: Patagonia, Argentina. Journal of Parasitology, 95(3), 646-651. Oxyuridae) in wild spider monkeys (Ateles geoffroyi) in tropical DOI: 10.1645/GE-1809.1 rain forest in Mexico: Morphological and molecular evidence. Sardella, N. H., & Fugassa, M. H. 2009b. Parasites in rodent Parasitology International, 64(5), 229-235. DOI: 10.1016/ coprolites from the historical archaeological site Alero j.parint.2015.02.006 Mazquiaran, Chubut Province, Argentina. Memórias do Stehli, F. G., & Webb, S. D. 1985. A kaleidoscope of plates, faunal Instituto Oswaldo Cruz, 104(1), 37-42. and floral dispersals, and sea level changes. In: Stehli, F.G.& Scheibel, R. P., Catzeflis, F., & Jiménez, F. A. 2014. The Webb, S.D., Eds.), The Great American Biotic Interchange. relationships of marsupial-dwelling Viannaiidae and pp. 3 - 16. New York: Plenum Press. description of Travassostrongylus scheibelorum n. sp. Thompson, J. N. 2005. The geographic mosaic of coevolution. (Trichostrongylina: Heligmosomoidea), from Chicago: University of Chicago Press:.p. 439. (Didelphidae) from French Guiana. Folia Parasitologica, 61(3), Tomassini, R. L., Montalvo, C. I., Ezquiaga, M. C.,2016. The 242-254. oldest record of flea/armadillos interaction as example of Siddiqui, M. A., & Kershaw, W. E. 1976. Host-parasite relations bioerosion on osteoderms from the late Miocene of the in filariasis II: The quantitative transmission of Argentine Pampas. International Journal of Paleopathology, Litomosoides carinii to Delhi and Carworth strains of white 15, 65-68. DOI: 10.1016/j.ijpp.2016.08.004 , including the effect of age Annals of Tropical Medicine Webb, S. D. 1978. A history of savanna vertebrates in the New and Parasitology, 70(3), 313-322. World. Part II: South America and the Great Interchange. Simões, R., Gentile, R., Rademaker, V., D’Andrea, P., Herrera, Annual Review of Ecology and Systematics, 9, 393-426. H., Freitas, T., Lanfredi, R., & Maldonado, A. 2010. Variation Weinstein, S. B., & Kuris, A. M., 2016. Independent origins of in the helminth community structure of pachyurus parasitism in Animalia. Biology Letters, 12(7). DOI: 10.1098/ (Rodentia: ) in two sub-regions of the Brazilian rsbl.2016.0324 Pantanal: the effects of land use and seasonality. Journal of Weirich, J.M., Catzeflis, F.M., Jiménez, F.A., 2016. Helminthology, 84(3), 266-275. DOI: 10.1017/ Guerrerostrongylus marginalis n. sp. (Trichostrongyloidea: S0022149X09990629 Heligmosomoidea) from the Guianan (Oecomys Simões, R. D., dos Santos, M. M., & Maldonado, A. 2012. A new auyantepui) from French Guiana. Parasite, 23(9), DOI: Heligmonellid (Nematoda: Heligmonellidae) from Oecomys 10.http://dx.doi.org/10.1051/parasite/2016009

Submitted: July 6 2016. Accepted: December 1st 2016.

Oecol. Aust., 21(1): 1-16, 2017