Matthew A. Wills

Pancrustacean Phylogeny in the Light of New Phylogenomic Data: Support for Remipedia as the Possible Sister Group of Hexapoda

Remipedes are a small and enigmatic group of crustaceans, first described only 30 years ago. Analyses of both morphological and molecular data have recently suggested a close relationship between Remipedia and Hexapoda. If true, the remipedes occupy an important position in pancrustacean evolution and may be pivotal for understanding the evolutionary history of crustaceans and hexapods. However, it is important to test this hypothesis using new data and new types of analytical approaches. Here, we assembled a phylogenomic data set of 131 taxa, incorporating newly generated 454 expressed sequence tag (EST) data from six species of crustaceans, representing five lineages (Remipedia, Laevicaudata, Spinicaudata, Ostracoda, and Malacostraca). This data set includes all crustacean species for which EST data are available (46 species), and our largest alignment encompasses 866,479 amino acid positions and 1,886 genes. A series of phylogenomic analyses was performed to evaluate pancrustacean relationships. We significantly improved the quality of our data for predicting putative orthologous genes and for generating data subsets by matrix reduction procedures, thereby improving the signal to noise ratio in the data. Eight different data sets were constructed, representing various combinations of orthologous genes, data subsets, and taxa. Our results demonstrate that the different ways to compile an initial data set of core orthologs and the selection of data subsets by matrix reduction can have marked effects on the reconstructed phylogenetic trees. Nonetheless, all eight data sets strongly support Pancrustacea with Remipedia as the sister group to Hexapoda. This is the first time that a sister group relationship of Remipedia and Hexapoda has been inferred using a comprehensive phylogenomic data set that is based on EST data. We also show that selecting data subsets with increased overall signal can help to identify and prevent artifacts in phylogenetic analyses.

A supertree approach to shorebird phylogeny.

BackgroundOrder Charadriiformes (shorebirds) is an ideal model group in which to study a wide range of behavioural, ecological and macroevolutionary processes across species. However, comparative studies depend on phylogeny to control for the effects of shared evolutionary history. Although numerous hypotheses have been presented for subsets of the Charadriiformes none to date include all recognised species. Here we use the matrix representation with parsimony method to produce the first fully inclusive supertree of Charadriiformes. We also provide preliminary estimates of ages for all nodes in the tree.ResultsThree main lineages are revealed: i) the plovers and allies; ii) the gulls and allies; and iii) the sandpipers and allies. The relative position of these clades is unresolved in the strict consensus tree but a 50% majority-rule consensus tree indicates that the sandpiper clade is sister group to the gulls and allies whilst the plover group is placed at the base of the tree. The overall topology is highly consistent with recent molecular hypotheses of shorebird phylogeny.ConclusionThe supertree hypothesis presented herein is (to our knowledge) the only complete phylogenetic hypothesis of all extant shorebirds. Despite concerns over the robustness of supertrees (see Discussion), we believe that it provides a valuable framework for testing numerous evolutionary hypotheses relating to the diversity of behaviour, ecology and life-history of the Charadriiformes.

The choice of model organisms in evo-devo.

Study of the model organisms of developmental biology was crucial in establishing evo–devo as a new discipline. However, it has been claimed that this limited sample of organisms paints a biased picture of the role of development in evolution. Consequently, judicious choice of new model organisms is necessary to provide a more balanced picture. The challenge is to determine the best criteria for choosing new model organisms, given limited resources.

Clades reach highest morphological disparity early in their evolution

There are few putative macroevolutionary trends or rules that withstand scrutiny. Here, we test and verify the purported tendency for animal clades to reach their maximum morphological variety relatively early in their evolutionary histories (early high disparity). We present a meta-analysis of 98 metazoan clades radiating throughout the Phanerozoic. The disparity profiles of groups through time are summarized in terms of their center of gravity (CG), with values above and below 0.50 indicating top- and bottom-heaviness, respectively. Clades that terminate at one of the “big five” mass extinction events tend to have truncated trajectories, with a significantly top-heavy CG distribution overall. The remaining 63 clades show the opposite tendency, with a significantly bottom-heavy mean CG (relatively early high disparity). Resampling tests are used to identify groups with a CG significantly above or below 0.50; clades not terminating at a mass extinction are three times more likely to be significantly bottom-heavy than top-heavy. Overall, there is no clear temporal trend in disparity profile shapes from the Cambrian to the Recent, and early high disparity is the predominant pattern throughout the Phanerozoic. Our results do not allow us to distinguish between ecological and developmental explanations for this phenomenon. To the extent that ecology has a role, however, the paucity of bottom-heavy clades radiating in the immediate wake of mass extinctions suggests that early high disparity more probably results from the evolution of key apomorphies at the base of clades rather than from physical drivers or catastrophic ecospace clearing.

Congruence Between Phylogeny and Stratigraphy: Randomization Tests and the Gap Excess Ratio

Stratigraphiccongruenceindices (e.g., stratigraphicconsistency index (SCI) of Huelsen- beck,1994,Paleobiology 40:563-569;relativecompleteness index (RCI) ofBenton,1994,TrendsEcol. Evol. 9:181-185 (not to be confused with the rescaled consistency index of Farris, 1989, Cladistics 5:417-419)) are increasingly being quoted for cladograms containing fossil taxa. However, like the character consistency index (CI, summed over all characters), these values cannot be compared for trees derived from different data sets. Just as the number of characters and taxa in data matrices affects typical CI values, so tree balance and the distribution of stratigraphic ranges (and indirectly tree size) delimit the range of congruence indices that can be obtained. Because investigators often seek tocomparetheperformanceof cladograms fromdifferentsources (e.g., differenttaxa, habitats, periods in history), indices of et insensitive to these factors are desirable. Two approaches are pro- posed here: (1) The gap excess ratio (GER) is a new metric thatcontrols for the distribution of range data but is sensitive to differences in tree balance. The GER expresses the difference between the minimum implied gap(MIG; the totalghostrangeimplied by a given set of stratigraphic ranges on agiven tree) and Gmin (the minimum possible ghost rangefor those data on any tree) as a fraction of the range of values possible for those stratigraphic data on any tree. Rather than reeecting inferred completeness of the fossil record (as does the RCI, which is only partially determined by cladistic constraints), the GER indicates congruence alone. (2) Randomization tests hold most potentially coneated parameters constant and compare the observed RCI or GER index with the distribution of indices obtained by randomly reassigning range data over the tree. This enables us to deduce whethertheMIGis signiecantlyless (i.e.,shows greater congruence)than for randompermutations of thesamerangedata.Stratigraphiccongruenceindices havebeen invoked as an ancillary criterion for assessing competing hypotheses of relationships derived from different sources or for choosing between equally parsimonous trees derived from the same character matrix. The erst application is illustrated with comparisons of actinopterygian and eutherian phylogenies, and the second is illustrated with a study of trees for fossil and Recent arthropods. (Ghost ranges; homoplasy ex- cess ratios; permutation tail probability; relative completeness index; retention index; stratigraphic consistency index.)

Morphological disparity: a primer

It has always been obvious that organisms have properties making them ‘different’ from each other. Historically, taxonomists have sought to register these differences and similarities by assigning species to subjectively-delimited groups within hierarchical classifications. Many current methods in sys-tematics still have a subjective component, and classifications often reflect biases inherent in their construction (Hull 1988).

Phylogeny of shorebirds, gulls, and alcids (Aves : Charadrii) from the cytochrome-b gene: parsimony, Bayesian inference, minimum evolution, and quartet puzzling

Charadrii (shorebirds, gulls, and alcids) have exceptional diversity in ecological, behavioral, and life-history traits. A phylogenetic framework is necessary to fully understand the relationships among these traits. Despite several attempts to resolve the phylogeny of the Charadrii, none have comprehensively utilized molecular sequence data. Complete and partial cytochrome-b gene sequences for 86 Charadrii and five Falconides species (as outgroup taxa) were obtained from GenBank and aligned. We analyzed the resulting matrices using parsimony, Bayesian inference, minimum evolution, and quartet puzzling methods. Posterior probabilities, decay indices, and bootstrapping provide strong support for four major lineages consisting of gulls, alcids, plovers, and sandpipers, respectively. The broad structure of the trees differ significantly from all previous hypotheses of Charadrii phylogeny in placing the plovers at the base of the tree below the sandpipers in a pectinate sequence towards a large clade of gulls and alcids. The parsimony, Bayesian, and minimum evolution models provide strong evidence for this phylogenetic hypothesis. This is further corroborated by non-tree based measures of support and conflict (Lento plots). The quartet puzzling trees are poorly resolved and inconclusive.

Fossilization causes organisms to appear erroneously primitive by distorting evolutionary trees

Fossils are vital for calibrating rates of molecular and morphological change through geological time, and are the only direct source of data documenting macroevolutionary transitions. Many evolutionary studies therefore require the robust phylogenetic placement of extinct organisms. Here, we demonstrate that the inevitable bias of the fossil record to preserve just hard, skeletal morphology systemically distorts phylogeny. Removal of soft part characters from 78 modern vertebrate and invertebrate morphological datasets resulted in significant changes to phylogenetic signal; it caused individual taxa to drift from their original position, predominately downward toward the root of their respective trees. This last bias could systematically inflate evolutionary rates inferred from molecular data because first fossil occurrences will not be recognised as such. Stem-ward slippage, whereby fundamental taphonomic biases cause fossils to be interpreted as erroneously primitive, is therefore a ubiquitous problem for all biologists attempting to infer macroevolutionary rates or sequences.

Increasing morphological complexity in multiple parallel lineages of the Crustacea

The prospect of finding macroevolutionary trends and rules in the history of life is tremendously appealing, but very few pervasive trends have been found. Here, we demonstrate a parallel increase in the morphological complexity of most of the deep lineages within a major clade. We focus on the Crustacea, measuring the morphological differentiation of limbs. First, we show a clear trend of increasing complexity among 66 free-living, ordinal-level taxa from the Phanerozoic fossil record. We next demonstrate that this trend is pervasive, occurring in 10 or 11 of 12 matched-pair comparisons (across five morphological diversity indices) between extinct Paleozoic and related Recent taxa. This clearly differentiates the pattern from the effects of lineage sorting. Furthermore, newly appearing taxa tend to have had more types of limbs and a higher degree of limb differentiation than the contemporaneous average, whereas those going extinct showed higher-than-average limb redundancy. Patterns of contemporary species diversity partially reflect the paleontological trend. These results provide a rare demonstration of a large-scale and probably driven trend occurring across multiple independent lineages and influencing both the form and number of species through deep time and in the present day.

The disparity of priapulid, archaeopriapulid and palaeoscolecid worms in the light of new data.

Priapulids and their extinct relatives, the archaeopriapulids and palaeoscolecids, are vermiform, carnivorous ecdysozoans with an armoured, extensible proboscis. These worms were an important component of marine communities during the Palaeozoic, but were especially abundant and diverse in the Cambrian. Today, they comprise just seven genera in four families. Priapulids were among the first groups used to test hypotheses concerning the morphological disparity of Cambrian fossils relative to the extant fauna. A previous study sampled at the generic level, concluding that Cambrian genera embodied marginally less morphological diversity than their extant counterparts. Here, we sample predominantly at the species level and include numerous fossils and some extant forms described in the last fifteen years. Empirical morphospaces for priapulids, archaeopriapulids and palaeoscolecids are relatively insensitive to changes in the taxon or character sample: their overall form has altered little, despite the markedly improved sampling. Cambrian and post‐Cambrian genera occupy adjacent rather than broadly overlapping regions of these spaces, and Cambrian species still show lower morphological disparity than their post‐Cambrian counterparts. Crucially, the significance of this difference has increased with improved taxon sampling over research time. In contrast with empirical morphospaces, the phylogeny of priapulids, archaeopriapulids and palaeoscolecids derived from morphological characters is extremely sensitive to details of taxon sampling and the manner in which characters are weighted. However, the extant Priapulidae and Halicryptidae invariably resolve as sister families, with this entire clade subsequently being sister group to the Maccabeidae. In our most inclusive trees, the extant Tubiluchidae are separated from these other living taxa by a number of small, intervening fossil clades.