Molecules, morphology, and ecology indicate a recent, amphibious ancestry for echidnas

Abstract

The semiaquatic platypus and terrestrial echidnas (spiny anteaters) are the only living egg-laying mammals (monotremes). The fossil record has provided few clues as to their origins and the evolution of their ecological specializations; however, recent reassignment of the Early Cretaceous Teinolophos and Steropodon to the platypus lineage implies that platypuses and echidnas diverged >112.5 million years ago, reinforcing the notion of monotremes as living fossils. This placement is based primarily on characters related to a single feature, the enlarged mandibular canal, which supplies blood vessels and dense electrosensory receptors to the platypus bill. Our reevaluation of the morphological data instead groups platypus and echidnas to the exclusion of Teinolophos and Steropodon and suggests that an enlarged mandibular canal is ancestral for monotremes (partly reversed in echidnas, in association with general mandibular reduction). A multigene evaluation of the echidna-platypus divergence using both a relaxed molecular clock and direct fossil calibrations reveals a recent split of 19-48 million years ago. Platypus-like monotremes (Monotrematum) predate this divergence, indicating that echidnas had aquatically foraging ancestors that reinvaded terrestrial ecosystems. This ecological shift and the associated radiation of echidnas represent a recent expansion of niche space despite potential competition from marsupials. Monotremes might have survived the invasion of marsupials into Australasia by exploiting ecological niches in which marsupials are restricted by their reproductive mode. Morphology, ecology, and molecular biology together indicate that Teinolophos and Steropodon are basal monotremes rather than platypus relatives, and that living monotremes are a relatively recent radiation.

Fig. 1.

Time scale of mammalian evolution (in Ma) as median (and 95% HPD) estimates from BEAST analyses for the combined nuclear and mitochondrial sequences (mtnuc₁₄). The (shaded) temporal window for the migration of marsupials into Australasia is 71–54.6 Ma. All nodes received Bayesian posterior probabilities of 1.00. Fossil calibrations were used at nodes indicated with an asterisk.

Fig. 2.

Substitution rates in substitutions/1,000 sites/Ma for the platypus (black circles), echidna (dotted circles), and monotreme stem (white circles) lineages, estimated using BEAST, for mt₈₈ (a and c) and nuc₁₄ (b and d). The age of monotremes was either unconstrained (a and b) or bounded by the age of Teinolophos (c and d). The substitution rates for each monotreme branch are compared with ranges for therian mammals (right vertical bar), sauropsids (left vertical bar), the overall mean (horizontal bar), and central 90% distribution (shaded). The y-axis is log-scaled.

Fig. 3.

Maximum parsimony bootstrap trees for extant (echidna and platypus) and extinct [Teinolophos (>112.5 Ma), Steropodon (≈105 Ma), and Obdurodon (from ≈25 Ma)] monotremes, based on analyses in which monotremes were either unconstrained phylogenetically or constrained to group within Australosphenida. Bootstrap percentages are shown for 4 analyses: morphol₄₃₉ unconstrained/morphol₄₄₁ unconstrained/morphol₄₃₉ constrained/morphol₄₄₁ constrained. (A) The reduced bootstrap consensus after Steropodon is pruned. (B) The bootstrap consensus for all taxa. An asterisk indicates that the clade was enforced. A total of 58 nonmonotreme taxa are not shown.