Conflict Resolution for Mesozoic Mammals: Reconciling Phylogenetic Incongruence Among Anatomical Regions

Abstract

The evolutionary history of Mesozoic mammaliaformes is well studied. Although the backbone of their phylogeny is well resolved, the placement of ecologically specialized groups has remained uncertain. Functional and developmental covariation has long been identified as an important source of phylogenetic error, yet combining incongruent morphological characters altogether is currently a common practice when reconstructing phylogenetic relationships. Ignoring incongruence may inflate the confidence in reconstructing relationships, particularly for the placement of highly derived and ecologically specialized taxa, such as among australosphenidans (particularly, crown monotremes), haramiyidans, and multituberculates. The alternative placement of these highly derived clades can alter the taxonomic constituency and temporal origin of the mammalian crown group. Based on prior hypotheses and correlated homoplasy analyses, we identified cheek teeth and shoulder girdle character complexes as having a high potential to introduce phylogenetic error. We showed that incongruence among mandibulodental, cranial, and postcranial anatomical partitions for the placement of the australosphenidans, haramiyids, and multituberculates could largely be explained by apparently non-phylogenetic covariance from cheek teeth and shoulder girdle characters. Excluding these character complexes brought agreement between anatomical regions and improved the confidence in tree topology. These results emphasize the importance of considering and ameliorating major sources of bias in morphological data, and we anticipate that these will be valuable for confidently integrating morphological and molecular data in phylogenetic and dating analyses.

Keywords: Mesozoic mammals; Multituberculata; australosphenida; correlated homoplasy; haramiyida; incongruence.

FIGURE 1

Workflow for calculating the maximum parsimony disadvantage for a data partition with the tree constrained to the total evidence topology, relative to unconstrained placements for taxa of interest (in this case, australosphenidans, multituberculates, and haramiyidans).

FIGURE 2

(A) NCDP₅₃₇ and (B) 51₅₃₇ phylogenies. The Bayesian inference topologies are shown, but with support values provided respectively for maximum parsimony-ordered (bootstrap), maximum likelihood (bootstrap), and Bayesian interference (Bayesian posterior probability) only for nodes at which at least one of these measures is < 95%. The asterisks indicate the constrained nodes (see Supplementary Material for the constraint used and Supplementary Figure S1 for the results from the unconstrained analyses). The dashes represent the branches which are not supported.

FIGURE 3

Bayesian inference marginal likelihood means and 95% higher posterior densities (averaged over two runs) for (A) NCDP₅₃₇, (B) 51₅₃₇, and (C) 51₃₅₀, with the tree topology linked and unlinked across the three anatomical regions. lnL advantage = (M_Llinked – M_Lunlinked)/M_Lunlinked.

FIGURE 4

Alternative phylogenetic positions for Haramiyida (green), Australosphenida (blue), and Multituberculata (orange) for the 51₅₃₇ and the 51₃₅₀ datasets on (A,E) all characters combined, and separately (B,F) mandibulodental, (C,G) cranial, and (D,H) postcranial. These groups were constrained to be monophyletic, given that some taxa that are informative for the placement of the group have too few characters for one or more anatomical regions. The maximum likelihood bootstrap (BP_ML) is represented only at nodes < 100%. The cranial trees are identical, since the same data is employed for this partition for both 51₅₃₇ and 51₃₅₀.

FIGURE 5

Monotreme placement. Kishino–Hasegawa tests (in IQ-TREE) for the alternative placements of Australosphenida on (A) the NCDP mammal backbone constraint phylogeny for the mandibulodental, cranial, and postcranial data for (B) the full character set and (C) excluding cheek teeth and shoulder girdle characters. The placement of Australosphenida is rejected in red (P < 0.05), not rejected in green (P > 0.1), and weakly rejected when not highlighted (P = 0.05–0.1). Placement 8 corresponds to the placement of Australosphenida within or adjacent to eutriconodonts and is inclusive of placements 7 and 8, and any placements with Jeholodens or Yanoconodon.

FIGURE 6

Maximum parsimony disadvantage for each sub-region (A) expressed as a percentage and regressed across sub-regions as a power curve and (B) corrected maximum parsimony disadvantage for those same values, but compared as a ratio relative to their expected values from the power curve regression.

FIGURE 7

Bayesian tree based on the 78₃₅₀ dataset. The Bayesian posterior probability (BPP) and maximum likelihood bootstrap (BP_ML) are represented only at nodes where BPP < 1 and BP_ML < 100%. The dashes represent branches which are not supported in the maximum likelihood analysis.