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The Classic Case of Cospeciation and Why Paradigms Are Important

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The Classic Case of Cospeciation and Why Paradigms Are Important University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Parasitology, Harold W. Manter Laboratory of Laboratory of Parasitology 2015 In the Eye of the Cyclops: The lC assic Case of Cospeciation and Why Paradigms Are Important Daniel R. Brooks University of Nebraska-Lincoln, [email protected] Eric P. Hoberg United States Department of Agriculture, Agricultural Research Service, [email protected] Walter A. Boeger Universidade Federal do Paraná, Brazil, [email protected] Follow this and additional works at: http://digitalcommons.unl.edu/parasitologyfacpubs Part of the Parasitology Commons Brooks, Daniel R.; Hoberg, Eric P.; and Boeger, Walter A., "In the Eye of the Cyclops: The lC assic Case of Cospeciation and Why Paradigms Are Important" (2015). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 778. http://digitalcommons.unl.edu/parasitologyfacpubs/778 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 Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Comp. Parasitol. 82(1), 2015, pp. 1–8 In the Eye of the Cyclops: The Classic Case of Cospeciation and Why Paradigms are Important 1,4 2 3 DANIEL R. BROOKS, ERIC P. HOBERG, AND WALTER A. BOEGER 1 H.W. Manter Laboratory of Parasitology, University of Nebraska State Museum of Natural History, University of Nebraska, Lincoln, Nebraska 68588-0514, U.S.A., 2 U.S. National Parasite Collection, Agricultural Research Service, USDA, Beltsville Area Research Center, BARC East 1180, Beltsville, Maryland 20705, U.S.A., (email: [email protected]), and 3 Laborato´rio de Ecologia Molecular e Parasitologia Evolutiva, Universidade Federal do Parana´, Caixa Postal 19073, Curitiba, PR 81531-980, Brazil (email: [email protected]) ABSTRACT: Scientific disagreements due to empirical problems—not enough data, not enough of the critical type of data, problems in analyzing the data—are generally short-lived and resolved in the next cycle of data production. Such disagreements are thus transitory in nature. Persistent scientific conflicts, on the other hand, do not necessarily mean some facts are correct and some are wrong, nor do they mean that we do not have enough information. More often, such persistent conflicts mean that the conceptual frameworks used by different groups of researchers are insufficient to resolve apparent conflicts in the data. The latter seems to be the case with persistent disagreements about the phenomenon of cospeciation, wherein there has historically been no framework that allows us to understand speciation by host switching when the host and parasite lineages involved are of equal ages. This situation can now be resolved with the emergence of what has become known as the ‘‘Stockholm Paradigm.’’ In short, re-examination of what has been dubbed the ‘‘classic case of cospeciation’’ shows that divergent views of cospeciation are subsumed and reconciled within the larger explanatory framework of the Stockholm Paradigm. The implications are considerable, given the need to have a fundamental understanding of faunal structure, assembly, and distribution in addition to an understanding of the historical and evolutionary drivers of diversity within the current arena of accelerating environmental change, ecological perturbation, and emerging infectious diseases. KEY WORDS: cospeciation, co-accommodation, Stockholm Paradigm, host switching, ecological fitting, taxon pulses, coevolution, pocket gophers, lice. Most parasitologists, like most scientists, under- embodied in the form of conceptual frameworks, take their research within conceptual frameworks that allows for the possible resolution of such conflicts they rarely, if ever, think about and that they never because it aids us in adjudicating data and, more question. This is not a novel insight, with philoso- importantly, because it helps us differentiate between phers of science having long noted that most apparent and real disagreements in our observations. scientists eschew philosophy while nevertheless In this commentary we discuss a case central to the relying heavily upon it to do their work. The usual comparative phylogenetic study of parasites and response by parasitologists to being questioned about coevolution in the context of such a philosophical the philosophical basis for their work is that they framework, that of parasite and host cospeciation. expect to collect such high-quality data that the data The implications are considerable, given the need to will ‘‘speak for themselves’’ and provide an answer to have a fundamental understanding of faunal structure, whatever problem they are investigating. Data, assembly, and distribution along with the historical however, rarely speak for themselves and, in fact, and evolutionary drivers of diversity in an arena of the very question of what constitutes valid data has a accelerating environmental change, ecological per- strong philosophical basis that is rarely acknowl- turbation, and emerging infectious diseases (for edged. As David Hull stated in his classic book recent reviews, see Brooks and Hoberg, 2013; Science as a Process (Hull, 1988), when scientists are Hoberg and Brooks, 2013; Brooks et al., 2014). in dispute, each side will claim that it can know what Brooks (1979) discussed two elements of parasite it needs to know (i.e., it can gather the essential data) evolution that could be examined phylogenetically. while the other side can never know what it needs to One of these was the extent to which parasite and know (i.e., cannot gather the proper data)—an host speciation events were correlated in space and approach that inevitably leads to conflict. Philosophy, time—for cases in which hosts and parasites speciated together, Brooks coined the term co- speciation. The other element of parasite evolution, 4 Corresponding author. which Brooks termed co-accommodation, had to do 1 2 COMPARATIVE PARASITOLOGY, 82(1), JANUARY 2015 Figure 1. Phylogenies of pocket gophers and lice (redrawn and modified from Hafner and Nadler, 1988, 1990) with phylogenetically incongruent nodes highlighted. Each of these represents a case of speciation by host-switching. with the evolution of the various parameters associ- (1979) as the source of the term cospeciation, with ated with host specificity (a subset of what Janzen good reason, as even a cursory comparison of the [1985] termed ecological fitting). Brooks made two phylogenetic trees published (Hafner and Nadler, fundamental assertions regarding these two elements: 1988) showed substantial points of disagreement, (1) cospeciation and co-accommodation were not the each of which according to the proposal by Brooks same thing so that, for example, presumptive host (1979) would have been interpreted as a case of specificity (especially host range) could not be used speciation by host switching and not cospeciation as a surrogate for cospeciation (and vice versa); and (Fig. 1). Hafner and Nadler (1990) subsequently (2) that cospeciation could only be documented by made it clear that two factors were more important finding congruence between host and parasite than either the congruence or incongruence of host speciation events in a phylogenetic comparison. In and parasite phylogenetic trees for their conception of short, cospeciation means that hosts and parasites are cospeciation. These factors were narrow host range the same age, and that departures from cospeciation and the equivalence of genetic divergence, which are episodes of speciation by host switching, in which Brooks (1979) had associated with co-accommoda- case the hosts and parasites are not of the same age. tion as opposed to cospeciation. Hafner and Nadler Nearly a decade after Brooks coined the term (1990) reasoned that parasite species limited to a cospeciation, Hafner and Nadler (1988) published a single host species, and host and parasite lineages phylogenetic analysis of a group of mammals and a exhibiting equivalent genetic divergence, must be the group of lice parasitizing them. After comparing the same age. Moreover, if they were of the same age, phylogenetic trees of each group based on molecular they then reasoned they must be the products of data and assessing the ages of the host and parasite cospeciation. Significantly, Hafner and Nadler (1990) lineages based on genetic divergence estimates, acknowledged that the genetic divergence data were Hafner and Nadler concluded that their work not actually equivalent but explained away the represented the best-documented case of cospeciation apparent discordance based on the assumptions that to date. However, these workers did not cite Brooks (1) the problem was due to discrepancies in the BROOKS ET AL.—IN THE EYE OF THE CYCLOPS: THE CLASSIC CASE OF COSPECIATION 3 parasite data, and (2) parasites had higher reproduc- reproductive rates are much higher than host tive rates, and thus accumulated mutations more reproductive rates (confounding reproductive rate rapidly, than did the hosts. It is at this point that with fecundity). Moreover, we know that host range complications begin to arise with their analysis. data for the majority of parasites species is heavily Because Hafner and Nadler (1990) already affected by sampling bias and also that phylogenetic ‘‘knew’’
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