A priori and a posteriori methods in comparative evolutionary studies of host–parasite associations

Abstract

Brooks parsimony analysis (BPA) and reconciliation methods in studies of host-parasite associations differ fundamentally, despite using the same null hypothesis. Reconciliation methods may eliminate or modify input data to maximize fit of single parasite clades to a null hypothesis of cospeciation, by invoking different a priori assumptions, including a known host phylogeny. By examining the degree of phylogenetic congruence among multiple parasite clades, using hosts as analogs of taxa but not presuming a host phylogeny or any degree of cospeciation a priori, BPA modifies the null hypothesis of cospeciation if necessary to maintain the integrity of the input data. Two exemplars illustrate critical empirical differences between reconciliation methods and BPA: (1) reconciliation methods rather than BPA may select the incorrect general host cladogram for a set of data from different clades of parasites, (2) BPA rather than reconciliation methods provides the most parsimonious interpretation of all available data, and (3) secondary BPA, proposed in 1990, when applied to data sets in which host-switching produces hosts with reticulate histories, provides the most parsimonious and biologically realistic interpretations of general host cladograms. The extent to which these general host cladograms, based on cospeciation among different parasite clades inhabiting the same hosts, correspond to host phylogeny can be tested, a posteriori, by comparison with a host phylogeny generated from nonparasite data. These observations lead to the conclusion that BPA and reconciliation methods are designed to implement different research programs based on different epistemologies. BPA is an a posteriori method that is designed to assess the host context of parasite speciation events, whereas reconciliation methods are a priori methods that are designed to fit parasite phylogenies to a host phylogeny. Host-switching events are essential for explaining complex histories of host-parasite associations. BPA assumes coevolutionary complexity (historical contingency), relying on parsimony as an a posteriori explanatory tool to summarize complex results, whereas reconciliation methods, which embody formalized assumptions of maximum cospeciation, are based on a priori conceptual parsimony. Modifications of basic reconciliation methods, embodied in TreeMap 1.0 and TreeMap 2.02, represent the addition of weighting schemes in which the researcher specifies allowed departures from cospeciation a priori, with the result that TreeMap results more closely agree with BPA results than do reconciled tree analysis results.

Reconstructing the Phylogeny

“…Combinatorially, these mechanisms correspond to subtree prune and regraft (SPR) operations [99]. Many techniques have been developed to compare gene trees [9][10][11][13][14][15][16][17] and host and parasite trees [19,22,100,101].…”

“…On the other hand, the methods that are used for the host-parasite analysis test whether there is a "significant" level of congruence between the trees. Since [18] (see a summary of works in [19] and the references within), there have been many studies analyzing host-parasite cospeciation. For example, the LRT (e.g., [20]), applying the Markov chain Monte Carlo (MCMC) techniques for estimating lateral transfers [21], methods that compare trees' pairwise distance matrices (e.g., by the Mantel test [22], ParaFit [23], and [24]), Brooks parsimony analysis (PSA) [25][26][27][28][29], and PSA [30] implemented in the software TreeMap [31,32] are statistical methods used to test for codivergence between trees.…”

The new orthogenesis

“…Comparisons between real BPA and model-based methods by researchers outside that program have always found in favor of BPA McLennan, 2001, 2003;Dowling, 2002;Dowling et al, 2003;Hoberg et al, 1997;Van Veller and Brooks, 2001). Other than the obvious issues of personal ambition, the only threatening thing about BPA is that, when applied to real examples, it postulates more host switching and less cospeciation than the maximum cospeciation program would wish to allow.…”

“…Why not allow as much host switching as the empirical data require, no more and no less? One could reply to this question by pointing out that all the modifications of methods used in maximum cospeciation analysis since 1990 have had the effect of allowing more explanations of host switching, in other words, of making those methods increasingly convergent and more BPA-like (see Dowling et al (2003) for a chronology). Why, then, do advocates of the maximum cospeciation program still claim that a model is necessary to arbitrate for the data rather than letting the data arbitrate among models, if they have been using empirical findings to modify their methods and determine the parameters in their models?…”

“…If true, this indicates the existence of different research programs studying phylogenetic aspects of coevolution, rather than different methods designed to perform the same function (Dowling et al, 2003;Van Veller and Brooks, 2001). In this light, we can see that RonquistÕs ''modified BPA'' was at least a good faith effort to turn BPA into something it was never designed to be-a model-based method.…”