Melanie J. Hopkins

Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution

Significance Biodiversification studies have often relied on constant-rate models of diversification. More recently, however, there has been an effort to identify changes in diversification rates within clades. This effort has largely focused on models of declining rates because many clades appear to have high initial rates, followed by slow-downs as ecological space fills. Here we provide an example of a 265 million-year-old marine invertebrate clade where evolutionary rates show a net increase over time instead. This is punctuated by intervals of high rates of morphological evolution, coinciding with major shifts in lifestyle and the evolution of new subclades. This study demonstrates the dynamic nature of evolutionary change within major clades. How ecological and morphological diversity accrues over geological time has been much debated by paleobiologists. Evidence from the fossil record suggests that many clades reach maximal diversity early in their evolutionary history, followed by a decline in evolutionary rates as ecological space fills or due to internal constraints. Here, we apply recently developed methods for estimating rates of morphological evolution during the post-Paleozoic history of a major invertebrate clade, the Echinoidea. Contrary to expectation, rates of evolution were lowest during the initial phase of diversification following the Permo-Triassic mass extinction and increased over time. Furthermore, although several subclades show high initial rates and net decreases in rates of evolution, consistent with “early bursts” of morphological diversification, at more inclusive taxonomic levels, these bursts appear as episodic peaks. Peak rates coincided with major shifts in ecological morphology, primarily associated with innovations in feeding strategies. Despite having similar numbers of species in today’s oceans, regular echinoids have accrued far less morphological diversity than irregular echinoids due to lower intrinsic rates of morphological evolution and less morphological innovation, the latter indicative of constrained or bounded evolution. These results indicate that rates of evolution are extremely heterogenous through time and their interpretation depends on the temporal and taxonomic scale of analysis.

Simple versus complex models of trait evolution and stasis as a response to environmental change

Significance Paleontologists have long argued about what the fossil record call tell us about how species evolve over long periods. Simple models such as stasis and random walks have been used to explore evolutionary patterns, but these have not always adequately captured the ways in which traits change over time in fossil species. Here we find that models with complex evolutionary dynamics are often favored, especially for fossil series that sample many populations, suggesting that the underlying evolutionary reality is likely more complex than represented by simplified—though still useful—models of trait change. Previous analyses of evolutionary patterns, or modes, in fossil lineages have focused overwhelmingly on three simple models: stasis, random walks, and directional evolution. Here we use likelihood methods to fit an expanded set of evolutionary models to a large compilation of ancestor–descendant series of populations from the fossil record. In addition to the standard three models, we assess more complex models with punctuations and shifts from one evolutionary mode to another. As in previous studies, we find that stasis is common in the fossil record, as is a strict version of stasis that entails no real evolutionary changes. Incidence of directional evolution is relatively low (13%), but higher than in previous studies because our analytical approach can more sensitively detect noisy trends. Complex evolutionary models are often favored, overwhelmingly so for sequences comprising many samples. This finding is consistent with evolutionary dynamics that are, in reality, more complex than any of the models we consider. Furthermore, the timing of shifts in evolutionary dynamics varies among traits measured from the same series. Finally, we use our empirical collection of evolutionary sequences and a long and highly resolved proxy for global climate to inform simulations in which traits adaptively track temperature changes over time. When realistically calibrated, we find that this simple model can reproduce important aspects of our paleontological results. We conclude that observed paleontological patterns, including the prevalence of stasis, need not be inconsistent with adaptive evolution, even in the face of unstable physical environments.

Comparing cal3 and other a posteriori time-scaling approaches in a case study with the pterocephaliid trilobites

Abstract. Reconstructing the tree of life involvesmore than identifying relationships among lineages; it also entails accurately estimating when lineages diverged. Paleontologists typically scale cladograms to time a posteriori by direct reference to first appearances of taxa in the stratigraphic record. Some approaches use probabilistic models of branching, extinction, and sampling processes to date samples of trees, such as the recently developed cal3 method, which stochastically draws divergence dates given a set of rates for those processes. However, these models require estimates of the rates of those processes, which may be hard to obtain, particularly for sampling. Here, we contrast the use of cal3 and other a posteriori time-scaling approaches by examining a previous study that documented a decelerating rate of morphological evolution in pterocephaliid trilobites. Although aspects of the data set make estimation of branching, extinction, and sampling rates difficult, we use a multifaceted approach to calculate and evaluate the rate estimates needed for applying cal3. In agreement with previous simulation studies, we find that the choice of phylogenetic dating method impacts downstream macroevolutionary conclusions. We also find contradictory evolutionary inferences between analyses on ancestor—descendant contrasts (based on ancestor trait reconstruction methods) and maximum-likelihood parameter estimates. Ancestral taxon inference in cal3 corroborates previously hypothesized ancestor—descendant sequences, but cal3 suggests greater support for budding cladogenesis than anagenesis. This case study demonstrates the potential and wide applicability of the cal3 method and the benefits afforded by choosing cal3 over simpler a posteriori time-scaling approaches.

Phylogenetic Paleoecology: Tree-Thinking and Ecology in Deep Time

The new and emerging field of phylogenetic paleoecology leverages the evolutionary relationships among species to explain temporal and spatial changes in species diversity, abundance, and distribution in deep time. This field is poised for rapid progress as knowledge of the evolutionary relationships among fossil species continues to expand. In particular, this approach will lend new insights to many of the longstanding questions in evolutionary biology, such as: the relationships among character change, ecology, and evolutionary rates; the processes that determine the evolutionary relationships among species within communities and along environmental gradients; and the phylogenetic signal underlying ecological selectivity in background and mass extinctions and in major evolutionary radiations.

Constraints on geographic variation in fiddler crabs (Ocypodidae: Uca) from the western Atlantic.

A key question in evolutionary biology is how intraspecific variation biases the evolution of a population and its divergence from other populations. Such constraints potentially limit the extent to which populations respond to selection, but may endure long enough to have macroevolutionary consequences. Previous studies have focused on the association between covariation patterns and divergence among isolated populations. Few have focused on geographic variation among semi‐connected populations, however, even though this may be indicative of early selective pressures that could lead to long‐term divergence and speciation. Here, we test whether covariation in the shape of the carapace of fiddler crabs (genus Uca Leach, 1814) is important for structuring geographic variation. We find that morphological divergence among populations is associated with evolvability in the direction of divergence in only a few species. The shape of the ancestral covariation matrix in these species differs from other species in having notably more variation concentrated along fewer directions (i.e. higher eccentricity). For most species, there is some evidence that covariation has constrained the range of directions into which populations have diverged but not the degree of divergence. These results suggest that even though fiddler crab populations have diverged morphologically in directions predicted by covariation, constraints on the extent to which divergence has occurred may only be manifested in species where variation patterns are eccentric enough to limit populations’ ability to respond effectively in many directions.

The oldest known digestive system consisting of both paired digestive glands and a crop from exceptionally preserved trilobites of the Guanshan Biota (Early Cambrian, China)

The early Cambrian Guanshan biota of eastern Yunnan, China, contains exceptionally preserved animals and algae. Most diverse and abundant are the arthropods, of which there are at least 11 species of trilobites represented by numerous specimens. Many trilobite specimens show soft-body preservation via iron oxide pseudomorphs of pyrite replacement. Here we describe digestive structures from two species of trilobite, Palaeolenus lantenoisi and Redlichia mansuyi. Multiple specimens of both species contain the preserved remains of an expanded stomach region (a “crop”) under the glabella, a structure which has not been observed in trilobites this old, despite numerous examples of trilobite gut traces from other Cambrian Lagerstätten. In addition, at least one specimen of Palaeolenus lantenoisi shows the preservation of an unusual combination of digestive structures: a crop and paired digestive glands along the alimentary tract. This combination of digestive structures has also never been observed in trilobites this old, and is rare in general, with prior evidence of it from one juvenile trilobite specimen from the late Cambrian Orsten fauna of Sweden and possibly one adult trilobite specimen from the Early Ordovician Fezouata Lagerstätte. The variation in the fidelity of preservation of digestive structures within and across different Lagerstätten may be due to variation in the type, quality, and point of digestion of food among specimens in addition to differences in mode of preservation. The presence and combination of these digestive features in the Guanshan trilobites contradicts current models of how the trilobite digestive system was structured and evolved over time. Most notably, the crop is not a derived structure as previously proposed, although it is possible that the relative size of the crop increased over the evolutionary history of the clade.

Non-linear ontogenetic shape change in Cryptolithus tesselatus (Trilobita) using three-dimensional geometric morphometrics

A decrease in the rate of cephalic shape change late in ontogeny has been documented for several species of trilobites, possibly associated with the cessation of segment release into the thorax. Qualitative descriptions of the ontogeny of Cryptolithus tesselatus Green, 1832, suggest that shape change in the cephalon was strongly influenced by the progressive accommodation of large funnel-shaped perforations (“fringepits”) over several molts. The number and arrangement of fringe-pits was established early in ontogeny, however, before thoracic segment release was completed. Due to the unusual and highly convex shape of the cephalon, we use three-dimensional (3D) geometric morphometrics to quantify shape change in this species and determine if there is a rate shift, and at what point in development this shift occurred. Three-dimensional morphometrics was made possible by extracting fixed and semi-landmarks from surface reconstructions of C. tesselatus rendered from CT scans of silicified specimens. Results show that the cephalon continued to change shape into adulthood, but that a threshold model with a rate shift associated with the cessation of new fringe-pits is best supported. 2D landmarks taken from the dorsal view fail to capture the dramatic change in convexity of the cephalon during development, but model comparison results are consistent with those based on the 3D landmark dataset, allowing comparison of this aspect of ontogenetic change with other species. Based on these comparisons, it appears that 1) trajectories are often better characterized by threshold models than simple linear regression models; 2) the timing of shifts may not be phylogeneti-

Development, Trait Evolution, and the Evolution of Development in Trilobites

Trilobites offer one of the best fossil records of any arthropod group. This is due to a number of factors, most notably the combination of (1) having inhabited areas where organisms are more likely to be buried and ultimately fossilized; and (2) having had a highly biomineralized exoskeleton more likely to survive the stresses of fossilization. This biomineralized exoskeleton was also morphologically complex, bearing traits that had ecological significance, and was present throughout postembryonic development, from larval to adult stages. Because the morphology of the exoskeleton changed gradually across molts during development, it is possible to reconstruct ontogenetic series for many species. Over the last decade, studies have documented both variation in modularity among closely related species and conserved developmental patterns among modules. In the latter case, trait evolution could still occur through modification of rates of morphological change along otherwise conserved ontogenetic trajectories. At the clade level, the pattern of expression and release of new exoskeletal segments during post-embryonic development was generally conserved across most species, but the relative timing of different segmentation events could vary, and developmental traits appear to have been relatively labile across the clades evolutionary history. Most recently, comparative analyses indicate that the association between segmentation events and the timing of shifts in the rate of ontogenetic shape change varies across species. Despite these advances, we still know relatively little about how development constrained or contributed to trait evolution in trilobites, and almost nothing about the origin of novel traits in trilobites. A major (but removable) obstacle is the current lack of well-supported trilobite phylogenies that span higher taxonomic levels.