A comprehensive and integrative reconstruction of evolutionary history for Anomura (Crustacea: Decapoda)

Abstract

Background: The infraorder Anomura has long captivated the attention of evolutionary biologists due to its impressive morphological diversity and ecological adaptations. To date, 2500 extant species have been described but phylogenetic relationships at high taxonomic levels remain unresolved. Here, we reconstruct the evolutionary history-phylogeny, divergence times, character evolution and diversification-of this speciose clade. For this purpose, we sequenced two mitochondrial (16S and 12S) and three nuclear (H3, 18S and 28S) markers for 19 of the 20 extant families, using traditional Sanger and next-generation 454 sequencing methods. Molecular data were combined with 156 morphological characters in order to estimate the largest anomuran phylogeny to date. The anomuran fossil record allowed us to incorporate 31 fossils for divergence time analyses.

Results: Our best phylogenetic hypothesis (morphological + molecular data) supports most anomuran superfamilies and families as monophyletic. However, three families and eleven genera are recovered as para- and polyphyletic. Divergence time analysis dates the origin of Anomura to the Late Permian ~259 (224-296) MYA with many of the present day families radiating during the Jurassic and Early Cretaceous. Ancestral state reconstruction suggests that carcinization occurred independently 3 times within the group. The invasion of freshwater and terrestrial environments both occurred between the Late Cretaceous and Tertiary. Diversification analyses found the speciation rate to be low across Anomura, and we identify 2 major changes in the tempo of diversification; the most significant at the base of a clade that includes the squat-lobster family Chirostylidae.

Conclusions: Our findings are compared against current classifications and previous hypotheses of anomuran relationships. Many families and genera appear to be poly- or paraphyletic suggesting a need for further taxonomic revisions at these levels. A divergence time analysis provides key insights into the origins of major lineages and events and the timing of morphological (body form) and ecological (habitat) transitions. Living anomuran biodiversity is the product of 2 major changes in the tempo of diversification; our initial insights suggest that the acquisition of a crab-like form did not act as a key innovation.

Figure 1

Combined Bayesian phylogram based on molecular (3669 characters) and morphological (156 characters) data. Vertical colored bars represent anomuran families, grey brackets represent superfamilies, and the black vertical line represents outgroups. Bayesian posterior probabilities represented as percentages and >70% are noted above or below branches.

Figure 2

Bayesian phylogram based on 5 genes 12S, 16S, 18S, 28S, H3 and 3669 characters. Vertical colored bars represent anomuran families, grey brackets represent superfamilies, and the black vertical line represents outgroups. Bayesian posterior probabilities represented as percentages and maximum likelihood bootstrap values are noted above or below branches.

Figure 3

Ancestral state reconstruction analysis using maximum likelihood methods for body shape and habitat transition within Anomura. Colored taxa correspond to anomuran families as noted in legend. Pie charts represent the likelihood of the ancestral state. (A) Character states for body shape were defined as crab-like white, squat lobster blue, symmetrical hermit green and asymmetrical hermit black. (B) Character states for habitat were defined as freshwater white, semi-terrestrial green, and marine black. Subtrees are shown for the transition into freshwater (Aeglidae) and semi-terrestrial habitats (Coenobitidae).

Figure 4

Divergence time chronogram using Bayesian evolutionary analysis by sampling trees using BEAST. Fossil calibration points are indicated by numbers 1–31 embedded in black circles (refer to Table 2). Divergence time estimates (MY) are noted adjacent to their respective nodes and blue nodal bars correspond to the 95% highest posterior density regions. Geological periods are superimposed onto the phylogeny and listed as follows: D, Devonian; C, Carboniferous; P, Permian; TR, Triassic; J, Jurassic; K, Cretaceous; T, Tertiary. Colored taxa correspond to anomuran families as noted in the legend. Green boxes indicate a diversification shift.