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Fossil Parasites See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/280091402 The Importance of Fossils in Understanding the Evolution of Parasites and Their Vectors Article in Advances in Parasitology · August 2015 DOI: 10.1016/bs.apar.2015.07.001 CITATIONS READS 39 8,901 2 authors: Kenneth De Baets D.T.J. Littlewood Friedrich-Alexander-University of Erlangen-Nürnberg Natural History Museum, London 130 PUBLICATIONS 1,494 CITATIONS 713 PUBLICATIONS 14,166 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Body-size dynamics and morphology of belemnites across the Pliensbachian-Toarcian crisis View project Zoo cases View project All content following this page was uploaded by Kenneth De Baets on 22 October 2017. The user has requested enhancement of the downloaded file. CHAPTER ONE The Importance of Fossils in Understanding the Evolution of Parasites and Their Vectors Kenneth De Baets*,1, D. Timothy J. Littlewoodx,1 *Fachgruppe Pal€aoUmwelt, GeoZentrum Nordbayern, Friedrich-Alexander-Universit€at Erlangen-Nurnberg,€ Erlangen, Germany xDepartment of Life Sciences, Natural History Museum, London, UK 1Corresponding authors: E-mail: [email protected]; [email protected] Contents 1. Introduction 2 2. Techniques for Ancient Parasite Discovery 4 2.1 Thin sections and computed tomography 5 2.2 Ancient biomolecules 6 2.2.1 Ancient DNA 6 2.2.2 Palaeoproteomics 7 3. The Parasite Fossil Record 8 3.1 Body fossils 14 3.2 Trace fossils and pathologies 18 3.3 Coprolites 22 4. Molecular Perspectives on Parasite Phylogeny and Evolution 26 4.1 Molecular clocks 29 4.2 HGT and ‘parasitic DNA’ 34 5. Future Perspectives 35 Acknowledgements 36 References 36 Abstract Knowledge concerning the diversity of parasitism and its reach across our current understanding of the tree of life has benefitted considerably from novel molecular phylogenetic methods. However, the timing of events and the resolution of the nature of the intimate relationships between parasites and their hosts in deep time remain problematic. Despite its vagaries, the fossil record provides the only direct evidence of parasites and parasitism in the fossil record of extant and extinct lineages. Here, we demonstrate the potential of the fossil record and other lines of geological evi- dence to calibrate the origin and evolution of parasitism by combining different kinds of dating evidence with novel molecular clock methodologies. Other novel methods promise to provide additional evidence for the presence or the life habit of pathogens Advances in Parasitology, Volume 90 ISSN 0065-308X © 2015 Elsevier Ltd. http://dx.doi.org/10.1016/bs.apar.2015.07.001 All rights reserved. 1 j 2 Kenneth De Baets and D. Timothy J. Littlewood and their vectors, including the discovery and analysis of ancient DNA and other bio- molecules, as well as computed tomographic methods. 1. INTRODUCTION Parasitism is one of the most successful modes of life, as evidenced by its convergent appearance in numerous lineages and its sheer absolute and relative abundance among extant biodiversity (Poulin and Morand, 2000). Antagonistic interactions, in the form of arms races between parasites and their hosts, have been considered important drivers of evolution (Zaman et al., 2014) and might also have contributed to the origin of sexual repro- duction (Mostowy and Engelst€adter, 2012). Because parasitism also has an obvious societal importance with many parasitic taxa being of significant biomedical, veterinary or economic importance (Bush et al., 2001), it is here that most of the research effort is focused. This focus is narrow and fails to provide the wider evolutionary picture or an appreciation of the influence of parasitism on, and as part of, biodiversity. Indeed, despite their importance and ubiquity, the evolutionary history of parasites is still poorly known, a phenomenon not helped by their inadequate, or rather inadequately explored, fossil record (Littlewood and Donovan, 2003). Establishing time-calibrated evolutionary frameworks to test the origins and radiations of parasites in parallel with studies on environmental param- eters, or the degree of coevolution between parasites and hosts, is a difficult but as yet a largely unexplored means by which ancient associations may be revealed. Parasitologists have often resorted to more circular lines of evi- dence, such as extrapolating from current host associations or distributions to put time constraints on the origins and evolution of parasites. For instance, where extant hosteparasite associations appear to be combinations of early divergent hosts and early divergent parasites, it is tempting and compelling to assume a long and ancient association; for example, early divergent gyroco- tylidean cestodes found only parasitizing early divergent ‘primitive’ holoce- phalan fishes (Xylander, 2001). In these cases, when the timing of a host’s divergence can be estimated from molecular or preferably fossil evidence, a calibration point for the parasite’s association also appears tractable, at least as a working hypothesis. Assumptions of cophylogeny are common but bring their own suites of problems, not in the least because of the traps set by multiple assumptions (Page, 2003). To reveal coevolutionary patterns, phylogenies of hosts and parasites need to be untangled to better understand The Importance of Fossils in the Evolution of Parasites 3 historical relationships, but the task is complex. Accurate estimates of histor- ical events such as co-divergence, duplication or loss of an association require complex mathematics and computationally demanding algorithms, and any estimate is contingent upon adequate sampling (Charleston and Perkins, 2006). Usually such sampling relies on phylogenies determined from extant organisms and pays little heed to loss of lineages through extinction. Whilst these studies can be profitable, direct evidence from the fossil record remains the most compelling evidence for past historical and deep evolutionary associations, as well as extinctions. Palaeontological data could also have a bearing on testing of how parasiteehost associations respond to environ- mental changes across longer time-scales and to what extent parasites could be prone to (co)extinction (Dunn et al., 2009). The past decades have seen a wealth of new discoveries, ranging from exceptionally preserved parasites and eggs assignable to modern (even family level) lineages (Cressey and Boxshall, 1989; Da Silva et al., 2014; Hugot et al., 2014), to characteristic traces of preserved biomolecules in host remains (Dittmar, 2009; Greenwalt et al., 2013; Wood et al., 2013b). Of particular note have been advances in X-ray, ion, electron and laser-beam techniques, serial grinding/imaging techniques and magnetic resonance tomography characterizing fine structures, textures and underlying chemis- tries (Mietchen et al., 2008; Sutton, 2008; Schiffbauer and Xiao, 2011; Dunlop et al., 2012; Cunningham et al., 2014a,b; Sutton et al., 2014). Addi- tionally, advances in mass spectrometry have allowed the detection and characterization of amino acid traces, particularly collagen within bone, to a remarkable level of detail and resolution (Cappellini et al., 2014). Such techniques open up the prospect of detecting traces of parasites and para- sitism more frequently and revealing key systematic features and morpho- logical characters indicative of a parasitic way of life. Another facet of palaeoparasitology, although perhaps not widely considered as such, is the study of horizontally (laterally) transferred DNA including transposable elements, where DNA from one organism can be detected buried within the genome of another. These so-called ‘genomic fossils’ offer clues as to the origins and nature of ancient associa- tions (Gilbert and Feschotte, 2010; Gilbert et al., 2010; Katzourakis and Gifford, 2010; Katzourakis, 2013; Koutsovoulos et al., 2014). Indeed, Ford Doolittle considers horizontally transferred DNA fragments as ‘basically parasites’ (p. 8; Gitschier, 2015)thathavebeenpartsoftheir host genomes for a considerable length of time. The rise in genome studies has provided ever-increasing evidence for horizontal gene transfers, HGTs 4 Kenneth De Baets and D. Timothy J. Littlewood (e.g. see Scholl et al., 2003), although such events detected among Metazoa appear to be more common in some groups (e.g. bdelloid rotifers: Gladyshev et al., 2008) than in others. Whereas palaeontology looks towards the earth’s fossil and subfossil record for ancient biotic interactions, it is clear that genomes may also be gleaned for evidence of relictual genetic elements of nonhost (“parasitic”)origin. Regardless of approach, time points gathered directly from fossils or inferred from calibrated phylogenies remain critical in understanding when, where and to some extent how hosteparasite interactions took place and how they might respond in the future; for example, the exchange of genes from parasitic to host plants of the genus Plantago has been shown to be a result of their direct physical contact with one another (Mower et al., 2004). Parasitic plants offer a particularly rich resource for understand- ing HGT (Davis and Xi, 2015). Morphologically based classifications of parasites have proved chal- lenging due to frequent apparent simplifications, convergence or specializa- tions in their morphology that make homology assessment difficult. However, novel molecular methods, used with caution,
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