© 2008 Society of Systematic Biologists
Morphology and Placental Mammal Phylogeny
Edited by Mark Hafner
1 Department of Biology, University of California Riverside, CA 92521, USA; E-mail: mark.springer{at}ucr.edu (M.S.S.)
2 Faculdade de Biociencias, PUCRS Porto Alegre, RS 90619-900, Brazil
3 School of Biological and Environmental Sciences, University College Dublin Belfield Dublin, 4, Ireland
4 Department of Veterinary Integrative Biosciences, Texas A&M University College Station, TX 77843-4458, USA
Received January 23, 2008; Revised February 4, 2008; Accepted March 14, 2008 In a recent article on placental mammal phylogeny (Springer et al., 2007), we discussed evidence for correlated character evolution among morphological characters. We also performed pseudoextinction analyses that assessed whether placental orders remained in the expected superordinal group (Afrotheria, Xenarthra, Euarchontoglires, Laurasiatheria) when molecular and soft-tissue data were coded as missing and only osteological data from Asher et al. (2003) remained for the pseudoextinct taxa. Finally, we examined congruence among 21 molecular data partitions and Asher et al.'s (2003) morphological data. Our results demonstrated that most placental orders moved to a different superordinal group when treated as pseudoextinct and also that Asher et al.'s (2003) morphological data consistently emerged as the most incongruent data partition. Based on these results, we questioned the ability of current morphological data sets and phylogenetic methods to reconstruct higher level relationships among placental mammals. In their response to our paper, Asher et al. (2008) raise several objections including (1) continued debate over our "preferred 4-clade topology" (p. 311) that renders our conclusions on morphology "premature" (p. 311); (2) basing our conclusions "on a single morphological data set" (p. 312); (3) our use of pseudoextinction techniques "to make broad generalizations about the quality of data for mammal phylogeny reconstruction" (p. 313); and (4) our conditional acknowledgement of the primacy "of morphological data to infer phylogeny of fossil taxa" (p. 313). Asher et al. (2008) make a number of useful points, but as discussed below these do not diminish the main conclusions of our earlier paper.
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Congruence and the Major Clades of Placental Mammals |
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We agree with Asher et al. (2008) that the placental tree is not fully resolved and that debate continues to surround local polytomies such as the root of the placental tree. Some recent molecular studies (Cannarozzi et al., 2007; Huttley et al., 2007) contradict one or more of the four major clades, but these studies typically have sparse taxon sampling for key taxa such as murid rodents that have accelerated rates of molecular evolution. Phylogenetic analyses that only include one or two murid rodents are especially susceptible to long-branch attraction and typically root the placental tree on the long murid branch. Indeed, this problem has long plagued molecular studies of placental mammal phylogeny and is the basis for the "guinea pig is not a rodent" phenomenon (D'Erchia et al., 1996). Nuclear and mitogenomic studies with adequate taxon sampling recover the four clades listed earlier with robust support. Analyses of nuclear genes that support the four clades include Madsen et al. (2001), Murphy et al. (2001a, 2001b), Scally et al. (2001), Waddell et al. (2001), Delsuc et al. (2002), Amrine-Madsen et al. (2003), Fleming et al. (2003), Waddell and Shelley (2003), Roca et al. (2004), Hallstrom et al. (2007), Nikolaev et al. (2007), and Wildman et al. (2007). Analyses of mitochondrial genes that support the four clades include Hudelot et al. (2003), Waddell and Shelley (2003), Reyes et al. (2004), Kitazoe et al. (2005), and Kjer and Honeycutt (2007). Each of the four clades is also supported by a wealth of indels and retrotransposon insertions (van Dijk et al., 1999; Poux et al., 2002, de Jong et al., 2003; Thomas et al., 2003; Murphy et al., 2004; Springer et al., 2004; Kriegs et al., 2006; Nishihara et al., 2006; Waters et al., 2007). Transposable element insertions are particularly compelling, especially when they corroborate previously well-supported hypotheses based on other types of data. Unlike analyses based on nucleotide sequences, studies of transposable elements are not expected to suffer from long-branch attraction (Lunter, 2007). We maintain that robust, independent support from nuclear, mitogenomic, and genomic analyses make the four clades among the best-supported groups in all of mammalian classification and also that these clades provide an appropriate benchmark for gauging the reliability of morphological characters in higher level placental phylogenetics. Asher et al. (2008: 312) imply that Springer et al. (2001) may support the association of Chiroptera + Dermoptera as sister taxa and consequently reject the four-clade hypothesis based on Springer et al.'s (2001) analysis of a morphological data set (Simmons and Geisler, 1998) that contained only archontan taxa. Springer et al. (2001) were aware of the potential homoplasy in using flying lemurs as an outgroup to bats; however, they had no choice but to use this data set as it was the most extensive morphological data set for bats at the time. Indeed, Gunnel and Simmons (2005) were also aware of this potential problem and expanded the Simmons and Geisler (1998) data set by scoring more laurasiatherian outgroups for bats.
Asher et al.'s (2008: 311) criticism that we used a "single topology to question an entire class of data (e.g., ‘morphology’) as premature" is a misinterpretation of our results. Our pseudoextinction analyses were not dependent on a single topology. Rather, analyses that treated single orders as pseudoextinct assessed "whether each pseudoextinct order was recovered as monophyletic" and also whether "each pseudoextinct order remained in the same superordinal group (Afrotheria, Xenarthra, Laurasiatheria, Euarchontoglires) as in Figure 1 or moved elsewhere on the tree" (Springer et al. 2007:676). Both intraordinal and interordinal relationships were free to vary in pseudoextinction analyses and were not constrained to follow the topology shown in our Figure 1. Data congruence analyses were based on comparisons of the shortest tree(s) for 22 different data partitions. The finding that morphological data consistently emerged as the most incongruent data partition is not dependent on a single topology.
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Asher et al. (2008) argue that some individual genes (e.g., VWF) fail to support the four-clade classification of placental mammals and suggest that these genes should not be eschewed just as morphology should not be eschewed. This comparison between individual genes and morphology ignores a fundamental difference between single genes and Asher et al.'s (2003) morphological data set. Namely, that single genes, whether they support the four-clade classification or not, remain more congruent with each other than they do with morphology. This is evident from figure 2 in Springer et al. (2007). Further, robust support for the four-clade classification is recovered when individual genes that fail to support the four-clade classification are analyzed together. This is precisely what we should expect if phylogentic signal is embedded in a background of random homoplastic noise. That is, we expect that random noise will sometimes exceed phylogenetic signal for finite data and that this problem will be more acute as the number of informative characters decreases and also for increasingly shorter internal branches. However, if background noise is random, then phylogenetic signal will overcome this noise as the data set becomes larger (e.g., single genes are concatenated into multigene data sets). Short internal branches will typically require more data for phylogenetic signal to overcome random noise. In contrast to phylogenetic signal against a backdrop of random, homoplastic noise, pervasive correlated character evolution in response to developmental constraints and/or ecological venue may be decidedly nonrandom and generate competing signal that is not overcome by phylogenetic signal simply by adding more and more characters to the data set. There is no doubt that morphology contains phylogenetic signal at the level of interordinal relationships (e.g., Paenungulata, Glires). However, the emerging pattern of incongruence between morphological and molecular data (Springer et al., 2007: fig. 2), in conjunction with numerous instances of ecological vicars that group together on published morphological trees (e.g., Shoshani and McKenna, 1998: fig. 1; Asher et al., 2003: fig. 4; Horovitz et al., 2004: fig. 1), suggest that morphological data contain a mixture of homologous characters and correlated homoplastic characters that are not effectively separated from each other by current phylogenetic methods.
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Use of a Single Morphological Data Set |
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We chose to analyze the Asher et al. (2003) data set because it was the largest available morphological data set to include representatives of all extant orders of placental mammals. Asher et al.'s (2003) data set was ideally suited for making comparisons with our molecular data because Asher et al. (2003: 132) selected extant taxa "based on the degree to which each was represented by the 22 genes used in Murphy et al. (2001b), most of which were in turn first published by Madsen et al. (2001) and Murphy et al. (2001a)." Asher et al. (2008) object that our conclusions are based on a single data set and suggest several other recent data sets (i.e., Horovitz, 2004; Luo and Wible, 2005; Wible et al., 2007) that may be appropriate for making comparisons. None of these data sets was collected with the explicit intention to maximize taxonomic overlap with the molecular data of Murphy et al. (2001b). All of these data sets also are missing representation from one or more placental orders. Most perplexing is the taxon sampling in Wible et al. (2007), which notably excludes four placental orders (Chiroptera, Dermoptera, Perissodactyla, and Pholidota) that were present in Asher et al. (2003). These same orders were identified by our pseudoextinction analyses to be among the most problematic, and all four moved to different superordinal groups in the analyses. Wible et al. (2007) provide no explanation for these missing representatives, but results of our pseudoextinction analyses suggest that inclusion of these taxa would likely have rendered all four, rather than just two, of the molecular-defined clades poly-or paraphyletic in their study.
Horovitz (2004) is the most complete of the data sets cited by Asher et al. (2008) and shares 30 placental taxa with Springer et al. (2007). We performed congruence analyses for 13 of the 20 nuclear genes in Springer et al. (2007) and the postcranial data set of Horovitz (2004) using our previously described methodology. Morphological data once again emerged as the most incongruent data partition after standardizing partitions so that they contained the same number of informative characters (Fig. 1). We also performed congruence tests that compared molecular sequences for five nuclear genes (APOB, RAG1, BRCA1, VWF, IRBP) to three different morphological data sets for marsupials (Horovitz and Sánchez-Villagra, 2003; Luo et al., 2003; Sánchez-Villagra et al., 2007) that include representation for the seven extant marsupial orders and obtained results that are similar to those for our comparisons involving placental mammals (Meredith, 2007). Thus, the pattern of incongruence between molecular and morphological data extends beyond Asher et al.'s (2003) morphological data set to other higher level morphological data sets for both placentals and marsupials. The morphological data sets that we have examined for congruence with molecular data are limited to osteological data and it remains possible that soft-tissue morphological characters will prove more compatible with molecular data. Nevertheless, osteological characters are the primary type of data that are available for fossil mammals.
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Pseudoexintction Techniques |
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Asher et al. (2008 : 313) argue that pseudoextinction "can be used to roughly gauge the performance of a subset of data in placing extinct taxa in a phylogeny, but is insufficient to make broad generalizations about the quality of data for mammal phylogeny reconstruction." In support of their conclusion, Asher et al. point out that "morphology is reliable in recognizing orders" (p. 313) and also that "some superordinal groups were first recognized at least in part (Archonta, Cetartiodactyla) or entirely (Glires, Paenungulata) on morphological evidence" (p. 313). Asher et al. are correct that most placental orders and some superordinal groups (e.g., Glires and Paenungulata) were first recognized based on morphology. Morphology clearly provides useful information for some mammalian superorders. However, our fundamental thesis is that morphological cladistic studies addressing higher level placental relationships conflate homology and homoplasy at the level of superordinal placental groups. This problem is not trivial based on our pseudoextinction analyses with Asher et al.'s (2003) morphological data set. Specifically, the majority of placental orders moved to a different superordinal group when molecular data were coded as missing and the four superordinal groups were never recovered as monophyletic. Minimally, this result demands careful consideration prior to combining molecular and morphological data to examine higher level placental relationships.
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Primacy of Morphology for Extinct Taxa |
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Morphological data are of fundamental importance for constructing hypotheses that place extinct mammals in a phylogenetic context. Asher et al. (2008) correctly note that morphology has not been fully exploited and also that morphological data "remain among the best (and often only) means by which we can incorporate the real data afforded to us via the fossil record into reconstructing the mammalian component of the Tree of Life" (p. 315). However, the primacy of morphological data for reconstructing relationships of extinct forms does not excuse morphology from critical assessments of its performance in analyses of higher level placental mammal phylogenetics. A robust solution for the mammalian component of the Tree of Life that includes living and extinct taxa must address problems of incongruence between molecular and morphological data and potential problems of correlated homoplasy among morphological characters. The problem of teasing homplastic morphological markers from homologous morphological markers will not simply disappear if it is ignored.
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Acknowledgments |
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M.S.S. and W.J.M. acknowledge support from NSF AToL program. We thank Dr. Ines Horovitz for providing her 2004 data set in nexus format. Mark Hafner and Jack Sullivan provided helpful comments on this manuscript.
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