Beyond Congruence: Evidential Integration and Inferring the Best Evolutionary Scenario

Molecular methods have revolutionised virtually every area of biology, and metazoan phylogenetics is no exception: molecular phylogenies, molecular clocks, comparative phylogenomics, and developmental genetics have collectively transformed our understanding of the evolutionary history of animals. Moreover, the diversity of methods and models within molecular phylogenetics has resulted in significant disagreement among molecular phylogenies as well as between these and traditional phylogenies. Here, I argue that tackling this multifaceted problem lies in integrating evidence to infer the best evolutionary scenario. I begin with an overview of recent developments in early metazoan phylogenetics, followed by a discussion of key conceptual issues in phylogenetics revolving around phylogenetic evidence and theory. I then argue that integration of different kinds of evidence is necessary for arriving at the best evolutionary scenario rather than the best-fitting cladogram. Finally, I discuss the prospects of this view in stimulating interdisciplinary cross-talk in early metazoan research and beyond.

Developmental processes in Ediacara macrofossils

The Ediacara Biota preserves the oldest fossil evidence of abundant, complex metazoans. Despite their significance, assigning individual taxa to specific phylogenetic groups has proved problematic. To better understand these forms, we identify developmentally controlled characters in representative taxa from the Ediacaran White Sea assemblage and compare them with the regulatory tools underlying similar traits in modern organisms. This analysis demonstrates that the genetic pathways for multicellularity, axial polarity, musculature, and a nervous system were likely present in some of these early animals. Equally meaningful is the absence of evidence for major differentiation of macroscopic body units, including distinct organs, localized sensory machinery or appendages. Together these traits help to better constrain the phylogenetic position of several key Ediacara taxa and inform our views of early metazoan evolution. An apparent lack of heads with concentrated sensory machinery or ventral nerve cords in such taxa supports the hypothesis that these evolved independently in disparate bilaterian clades.

A screen for gene paralogies delineating evolutionary branching order of early Metazoa

The evolutionary diversification of animals is one of Earth’s greatest triumphs, yet its origins are still shrouded in mystery. Animals, the monophyletic clade known as Metazoa, evolved wildly divergent multicellular life strategies featuring ciliated sensory epithelia. In many lineages epithelial sensoria became coupled to increasingly complex nervous systems. Currently, different phylogenetic analyses of single-copy genes support mutually-exclusive possibilities that either Porifera or Ctenophora is sister to all other animals. Resolving this dilemma would advance the ecological and evolutionary understanding of the first animals and the evolution of nervous systems. Here we describe a comparative phylogenetic approach based on gene duplications. We computationally identify and analyze gene families with early metazoan duplications using an approach that mitigates apparent gene loss resulting from the miscalling of paralogs. In the transmembrane channel-like (TMC) family of mechano-transducing channels, we find ancient duplications that define separate clades for Eumetazoa (Placozoa + Cnidaria + Bilateria) versus Ctenophora, and one duplication that is shared only by Eumetazoa and Porifera. In the MLX/MLXIP family of bHLH-ZIP regulators of metabolism, we find that all major lineages from Eumetazoa and Porifera (sponges) share a duplication, absent in Ctenophora. These results suggest a new avenue for deducing deep phylogeny by choosing rather than avoiding ancient gene paralogies.

Three-dimensionally preserved soft tissues and calcareous hexactins in a Silurian sponge: implications for early sponge evolution

Sponges (Porifera), as one of the earliest-branching animal phyla, are crucial for understanding early metazoan phylogeny. Recent studies of Lower Palaeozoic sponges have revealed a variety of character states and combinations unknown in extant taxa, challenging our views of early sponge morphology. The Herefordshire Konservat–Lagerstätte yields an abundant, diverse sponge fauna with three-dimensional preservation of spicules and soft tissue. Carduispongia pedicula gen. et sp. nov. possesses a single layer of hexactine spicules arranged in a regular orthogonal network. This spicule type and arrangement is characteristic of the reticulosans, which have traditionally been interpreted as early members of the extant siliceous Class Hexactinellida. However, the unusual preservation of the spicules of C . pedicula reveals an originally calcareous composition, which would be diagnostic of the living Class Calcarea. The soft tissue architecture closely resembles the complex sylleibid or leuconid structure seen in some modern calcareans and homoscleromorphs. This combination of features strongly supports a skeletal continuum between primitive calcareans and hexactinellid siliceans, indicating that the last common ancestor of Porifera was a spiculate, solitary, vasiform animal with a thin skeletal wall.

Cell signalling stabilizes morphogenesis against noise

Embryonic development involves gene networks, extracellular signaling, cell behaviors (cell division, apoptosis, adhesion, etc.) and mechanical interactions. How should gene networks, extracellular signaling and cell behaviors be coordinated to lead to complex and robust morphologies?To explore this question, we randomly wired genes and cell behaviors into a huge number of networks in EmbryoMaker. EmbryoMaker is a general mathematical model of animal development that simulates how embryos change,i.e.how the 3D spatial position of cells change, over time due such networks. Real gene networks are not random. Random networks, however, allow an unbiased view on the requirements for complex and robust development.We found that the mere autonomous activation of cell behaviors, especially cell division and contraction, was able to lead to the development of complex morphologies. We also found that complex morphologies tend to be less robust to noise than simple morphologies. However, we found that morphologies that developed through extracellular signaling and complex gene networks were, on average, more robust to noise. This stabilization occurs when gene networks and extracellular signaling partition the embryo into different regions where cell behaviors are regulated in slightly different ways. Our results are consistent with theories proposing that morphological complexity arose in early metazoan evolution as a consequence of the cell bio-mechanics already present in protozoa and that robustness evolved by the co-option of gene networks and extracellular cell signaling.

Unusually variable paleocommunity composition in the oldest metazoan fossil assemblages

Recent excavations of Ediacaran assemblages have revealed striking bed-to-bed variation in diversity–abundance structure, offering potential insight into the ecology and taphonomy of these poorly understood early Metazoan ecosystems. Here we compare faunal variability in Ediacaran assemblages to that of younger benthic assemblages, both fossil and modern. We decompose the diversity of local assemblages into within-collection (α) and among-collection (β) components and show that β diversity in Ediacaran assemblages is unusually high relative to younger assemblages. Average between-bed ecological dissimilarities in the Phanerozoic fossil record are comparable to within-habitat dissimilarities typically observed over meter to kilometer scales in modern benthic marine habitats, but dissimilarities in Ediacaran assemblages are comparable to those typically observed over 10–100 km scales in modern habitats. We suggest that the unusually variable diversity–abundance structure of Ediacaran assemblages is due both to their preservation as near snapshots of benthic communities and to original ecological differences, in particular the paucity of motile taxa and the near lack of predation and infaunalization.