Incongruence Between Morphological and Mitochondrial-DNA Characters Suggests Hybrid O rigins of Parthenogenetic Weevil Lineages ( Genus Aramigus ) B

Ð An expanded matrix of morphological characters for the genus Aramigus (Coleoptera: Curculionidae), which includes numerous polyploid parthenogenetic lineages, was compared and combined with a published matrix of mitochondrial DNA (mtDNA) characters. The matrix of morphological characters provides little resolution of the A. tessellatus and A. uruguayensis species complexes but does resolve previously unresolved relationships among other morphologically de® ned species (A. globoculus 1 A. intermedius, A. curtulus 1 A. planioculus). The morphological and mtDNA characters are signi® cantly incongruent (0 .435 IM 0 . 463; IM F 5 0 . 0735), according to the tests of Farris et al. (P 5 0 . 010) and Templeton (P < 0 . 005), probably because of hybrid origins of polyploid parthenogenetic lineages. For the few sexual lineages included in both matrices, morphology and mtDNA provide congruent estimates of phylogeny. In spite of recent injunctions against combining data sets that are incongruent because of di ering histories, the results of the combined analyses were used to select one of the most-parsimonious mtDNA trees as the best estimate of maternal-lineage genealogy and to reconstruct the evolution of parthenogenesis under the assumption that transitions from sexuality to parthenogenesis are irreversible. W here cytogenetically justi® ed, as in weevils, the irreversibility assumption is useful for producing conservative estimates of the age of parthenogenetic lineages in spite of potential sampling bias against sexuals. [Ancient asexuals; Entiminae; hybridization; incongruence; Naupactini; parthenogenesis; reticulation; root weevils. ] The rise of molecular systematics has been accompanied by a persistent controversy over how to interpret con ̄ icts between morphological and molecular characters (Paterson, 1987; Swo ord, 1991). O ne response to the problem has been the invention and growing use of statistical tests of character incongruence (Templeton, 1983; Larson, 1994; Farris et al., 1995; Poe, 1996), which often fail to reject the null hypothesis of homogeneity even when the trees from the separate analyses di er greatly (Sites et al., 1996). In some cases, however, the incongruence between morphological and molecular estimates has been found to be signi® cant (M iyamoto, 1996; Poe, 1996; Engel and Schultz, 1997). Explanations for such incongruence fall into two classes: (1) error in phylogenetic inference for one or both data sets, and (2) a di erence in phylogenetic history between the two data sets (de Q ueiroz et al., 1995). Error in phylogenetic inference is thought to result from convergence, particularly from convergences caused by very di erent rates of evolution between taxa (Sytsma, 1990; Kadereit, 1994). Di erences in phylogenetic history have been thought to result from errors in orthology assessment, from lineage sorting, or from reticulation (Sytsma, 1990; Soltis and Kuzo , 1995; Birky, 1996). In plants, reticulation has widely been thought to be important (M cDade, 1995). Incongruence between morphological and molecular characters in plant taxa has often been interpreted as having resulted from a history of reticulation (Sytsma, 1990; Soltis and Kuzo , 1995; Schilling and Panero, 1996). In contrast, in animals, cases of incongruence are more often ascribed to some sort of error (Miyamoto, 1996; Poe, 1996; Engel and Schultz, 1997). Parthenogenetic animal lineages represent a peculiar case. In vertebrates, almost every parthenogenetic lineage has now been shown to be of hybrid origin (Dawley and Bogart, 1989; Cole and Dessauer, 1993; Cole et al., 1993; Moritz, 1993; Cole et al., 1995; Radtkey et al., 1995). In parthenogenetic line475 D ow naded rom http/academ ic.p.com /sysbio/articlact/47/3/475/1703751 by gest on 23 M arch 2019 ages in other animal taxa, the importance of hybrid origins is far less clear, though the number of examples is growing (Dowling and Secor, 1997; Giessler, 1997; Parker and Niklasson, in press). For no parthenogenetic animals have molecular and morphological data sets been directly compared to look for patterns of incongruence. Here, we present a case of strong incongruence between morphological and mtDNA data sets for a genus of weevils (Aramigus) that includes a large number of parthenogenetic lineages, and we interpret this incongruence as likely to be the result of hybrid origins of parthenogenesis. It has been argued that when data sets are incongruent, and particularly when that incongruence is thought to re ̄ ect a di erence in phylogenetic history, the sets should not be combined (de Q ueiroz et al., 1995). However, we do perform combined analysis of our data, which we argue helps us to choose the best-supported estimate of maternal-lineage genealogy among the most-parsimonious mtDNA trees. The evolution of parthenogenetic lineages is of great theoretical interest to evolutionists because it bears directly on a major unsolved problem, the adaptive signi® cance of sexuality. A basic question is whether any parthenogenetic lineages have survived for very long periods, or whether all are of recent origin (M aynard Smith, 1992; Judson and Normark, 1996). Available phylogenetic data on this question have been subject to sharply di erent interpretations. We discuss the basis of this controversy , which hinges in part on the problem of adequate taxonomic sampling and in particular on the potential in some groups (such as Aramigus) for systematic underrepresentation of sexual lineages. To minimize the e ects of such bias and to produce conservative estimates of clonal antiquity, we invoke an assumption of irreversibility for transitions from sexuality to parthenogenesis, which we argue is reasonable, given the cytogenetic details of sexuality and parthenogenesis in weevils. M ATERIALS AND M ETHO DS