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, 38 (1), 43-62

Monophyly of Terrestrial Adephagan Beetles as Indicated by Three Nuclear Genes (Coleoptera: Carabidae and Trachypachidae)

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Monophyly of Terrestrial Adephagan Beetles as Indicated by Three Nuclear Genes (Coleoptera: Carabidae and Trachypachidae)

D R Maddison et al. Zool Scr.

Abstract

The beetle suborder Adephaga is traditionally divided into two sections on the basis of habitat, terrestrial Geadephaga and aquatic Hydradephaga. Monophyly of both groups is uncertain, and the relationship of the two groups has implications for inferring habitat transitions within Adephaga. Here we examine phylogenetic relationships of these groups using evidence provided by DNA sequences from all four suborders of beetles, including 60 species of Adephaga, four Archostemata, three Myxophaga, and ten Polyphaga. We studied 18S ribosomal DNA and 28S ribosomal DNA, aligned with consideration of secondary structure, as well as the nuclear protein-coding gene wingless. Independent and combined Bayesian, likelihood, and parsimony analyses of all three genes supported placement of Trachypachidae in a monophyletic Geadephaga, although for analyses of 28S rDNA and some parsimony analyses only if Coleoptera is constrained to be monophyletic. Most analyses showed limited support for the monophyly of Hydradephaga. Outside of Adephaga, there is support from the ribosomal genes for a sister group relationship between Adephaga and Polyphaga. Within the small number of sampled Polyphaga, analyses of 18S rDNA, wingless, and the combined matrix supports monophyly of Polyphaga exclusive of Scirtoidea. Unconstrained analyses of the evolution of habitat suggest that Adephaga was ancestrally aquatic with one transition to terrestrial. However, in analyses constrained to disallow changes from aquatic to terrestrial habitat, the phylogenies imply two origins of aquatic habit within Adephaga.

Figures

Fig. 1
Fig. 1
Representatives of the two living genera of trachypachids. Scale bar: 1 mm. A. Trachypachus holmbergi, USA: Oregon: Lincoln Co., Cape Perpetua Campground on route 101 S of Yachats, 44.2809°N 124.1014°W. B. Systolosoma breve, CHILE: Reg. IX: P.N. Nahuelbuta, 37.8042°S 73.0281°W.
Fig. 2
Fig. 2
Maximum likelihood tree inferred from all wingless amino acids (Opal alignment) under the constraint that Adephaga is monophyletic (striped branch). Arrow indicates placement of Polyphaga if constraint is not enforced. Branches with dots have Bayesian Posterior Probability of 0.90 or more for the Opal alignment of all amino acids. Branches that are slightly thickened have an additionally property, in that they appear in the most parsimonious trees. The thickest branches have, additionally, a parsimony bootstrap value of ≥ 80 for all nucleotides based upon the Opal alignment, a likelihood bootstrap value ≥ 80 for all Opal alignment amino acids, and a Bayesian Posterior Probability of 0.90 or more for the ModClustal alignment of all nucleotides. Dots and thickened branches are based upon unconstrained analyses. The Geadephaga branch is indicated by an asterisk.
Fig. 3
Fig. 3
Maximum likelihood tree inferred from 18S rDNA under the constraint that Adephaga is monophyletic (striped branch). Arrow indicates placement of Polyphaga (as sister to Hydradephaga excluding Gyrinidae) if the constraint is not enforced. Branches with dots have Bayesian Posterior Probability of 0.90 or more. Branches that are slightly thickened also appear in the most parsimonious trees. The thickest branches have, in addition, a parsimony bootstrap value of ≥ 80, a likelihood bootstrap value ≥ 80. Dots and thickened branches are based upon unconstrained analyses. The Geadephaga branch is indicated by an asterisk.
Fig. 4
Fig. 4
Maximum likelihood tree inferred from 28S rDNA under the constraint that Coleoptera is monophyletic. Arrow indicates placement of Oliarces and Mantispa if constraint is not enforced. Branches with dots have Bayesian Posterior Probability of 0.90 or more. Branches that are slightly thickened also appear in the most parsimonious trees. The thickest branches have, in addition, a parsimony bootstrap value of ≥ 80, a likelihood bootstrap value ≥ 80. Dots and thickened branches are based upon unconstrained analyses. The Geadephaga branch is indicated by an asterisk.
Fig. 5
Fig. 5
90% majority-rule consensus tree of 11,226 post-burn-in trees from the Bayesian analysis of the combined data matrix (wingless amino acids, excluding the indel-rich region, plus 18S rDNA and 28S rDNA), with Bayesian posterior probability estimates on each branch. The four slightly thickened branches are those clades that are strongly supported in two additional analyses with the combined nucleotide matrix (all wingless nucleotides, ModClustal alignment, plus 18S rDNA and 28S rDNA): a Bayesian Posterior Probability of 0.80 or more, and a likelihood bootstrap value of 80 or more. The moderately thick, gray branches indicate clades that are strongly supported in those analyses in addition to having a parsimony bootstrap value ≥ 80 for the combined nucleotide matrix (with Coleoptera constrained to be monophyletic). The ten very thick branches are strongly supported in the same way, and in addition show strong support from each of the three genes independently (for each gene BPP≥90, and in MPTs; for 28S rDNA with Coleoptera constrained to be monophyletic and for wingless with Adephaga constrained to be monophyletic). The Geadephaga branch is indicated by an asterisk.
Fig. 6
Fig. 6
Maximum likelihood tree inferred from mitochondrial 16S rDNA, under the constraint that Adephaga is monophyletic (striped branch). If this constraint is not enforced, then Polyphaga is the sister of the carabid genus Elaphrus. Branches with dots have Bayesian Posterior Probability of 0.90 or more. Branches that are slightly thickened in addition appear in the most parsimonious trees. The thickest branches have in addition a parsimony bootstrap value of ≥ 80, a likelihood bootstrap value ≥ 80. Dots and thickened branches are based upon unconstrained analyses.
Fig. 7
Fig. 7
Summary of support for monophyly of (A) Geadephaga and (B) Hydradephaga. Each row represents a different matrix, each column a different analysis. Dark squares indicate support for the clade for that matrix and analysis; white squares indicate lack of support or support for non-monophyly. Matrices: “wg aa”: all wingless amino acids, Opal alignment; “wg nuc”: all wingless nucleotides, ModClustal alignment; “18S”: 18S rDNA; “28S”: 28S rDNA; “wg aa + 18S + 28S”: combined matrix of wingless amino acids (Opal alignment, excluding indel-rich region), 18S rDNA, and 28S rDNA; “wg nuc + 18S + 28S”: combined matrix of all wingless nucleotides (ModClustal alignment), 18S rDNA, and 28S rDNA. 16S mt rDNA: mitochondrial 16S rDNA data from Hunt et al. (2007). Analyses: “Bay”: Bayesian Posterior Probability of clade (if cell is dark) or of contradictory clade (if cell is white); “ML”: Maximum Likelihood Tree; “MLB”: Maximum Likelihood Bootstrap value; “P”: Most Parsimonious Trees; “PB”: Parsimony Bootstrap value. ?: No support for or against the clade; x: contradictory clade present; *: analysis done enforcing monophyly of Coleoptera; a: analysis done enforcing monophyly of Adephaga.
Fig. 8
Fig. 8
Habitats of two species of trachypachids. A. Trachypachus slevini, USA: Oregon: Lincoln Co., Moolack Beach, 44.7093°N 124.0605°W. B. Systolosoma breve, CHILE: Reg. IX: Rio Pedregoso, E of El Pastal, 646m, 39.1676°S 72.0001°W. Trachypachids were found in areas indicated by arrows, on the slope of material eroded from the neighboring bank.

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