Evolutionary theory and systematics: relationships between process and patterns

The relevance of the Modern Evolutionary Synthesis to the foundations of taxonomy (the construction of groups, both taxa and phyla) is reexamined. The nondimensional biological species concept, and not the multidimensional, taxonomic, species notion which is based on it, represents a culmination of an evolutionary understanding. It demonstrates how established evolutionary mechanisms acting on populations of sexually reproducing organisms provide the testable ontological basis of the species category. We question the ontology and epistemology of the phylogenetic or evolutionary species concept, and find it to be a fundamentally untenable one. We argue that at best, the phylogenetic species is a taxonomic species notion which is not a theoretical concept, and therefore should not serve as foundation for taxonomic theory in general, phylogenetics, and macroevolutionary reconstruction in particular. Although both evolutionary systematists and cladists are phylogeneticists, the reconstruction of the history of life is fundamentally different in these two approaches. We maintain that all method, including taxonomic ones, must fall out of well corroborated theory. In the case of taxonomic methodology the theoretical base must be evolutionary. The axiomatic assumptions that all phena, living and fossil, must be holophyletic taxa (species, and above), resulting from splitting events, and subsequently that evaluation of evolutionary change must be based on a taxic perspective codified by the Hennig ian taxonomic species notion, are not testable premises. We discuss the relationship between some biologically, and therefore taxonomically, significant patterns in nature, and the process dependence of these patterns. Process-free establishment of deductively tested “genealogies” is a contradiction in terms; it is impossible to “recover” phylogenetic patterns without the investment of causal and processual explanations of characters to establish well tested taxonomic properties of these (such as homologies, apomorphies, synapomorphies, or transformation series). Phylogenies of either characters or of taxa are historical-narrative explanations (H-N Es), based on both inductively formulated hypotheses and tested against objective, empirical evidence. We further discuss why construction of a “genealogy”, the alleged framework for “evolutionary reconstruction”, based on a taxic, cladistic outgroup comparison and a posteriori weighting of characters is circular. We define how the procedure called null-group comparison leads to the noncircular testing of the taxonomic properties of characters against which the group phylogenies must be tested. This is the only valid rooting procedure for either character or taxon evolution. While the Hennig -principle is obviously a sound deduction from the theory of descent, cladistic reconstruction of evolutionary history itself lacks a valid methodology for testing transformation hypotheses of both characters and species. We discuss why the paleontological method is part of comparative biology with a critical time dimension ana why we believe that an “ontogenetic method” is not valid. In our view, a merger of exclusive (causal and interactive, but best described as levels of organization) and inclusive (classificatory) hierarchies has not been accomplished by a taxic scheme of evolution advocated by some. Transformational change by its very nature is not classifiable in an inclusive hierarchy, and therefore no classification can fully reflect the causal and interactive chains of events constituting phylogeny, without ignoring and contradicting large areas of corroborated evolutionary theory. Attempts to equate progressive evolutionary change with taxic schemes by Haeckel were fundamentally flawed. His ideas found 19th century expression in a taxic perception of the evolutionary process (“phylogenesis”), a merger of typology, hierarchic and taxic notions of progress, all rooted in an ontogenetic view of phylogeny. The modern schemes of genealogical hierarchies, based on punctuation and a notion of “species” individuality, have yet to demonstrate that they hold promise beyond the Haeckel ian view of progressive evolution.     

Continental gateways and the dynamics of mammalian faunas

Continental gateways occur where mountainous topography interacts with changing climate and sea level to open or close dispersal corridors. The interaction of permeable or impermeable montane barriers with changing or stable climate yields four biogeographic states, each associated with changes in diversification rates and ecological structure of faunas. For example, permeable montane barriers and climatic stability result in low rates of immigration and extinction, elevated endemic speciation, and stable ecological structure. Three examples from the mammalian fossil record test these scenarios. (1) In Miocene faunas of Pakistan, immigration rates peaked and faunal proportions changed during an interval of cooling and open corridors. (2) In Miocene faunas of Spain, elevated extinction and origination rates and changing trophic structure occurred during regional aridification with open corridors. (3) In Quaternary faunas of South Africa, ungulates experienced range reductions and elevated extinction during the transition from glacial to interglacial climates as corridors closed.     

Ecological correlates and phylogenetic signal of host use in North American unionid mussels

Mussels in the order Unionoida comprise ～75% of the world’s freshwater bivalve species and are free-living apart from a brief larval stage that parasitizes fish. We investigated the relationships among species of North American unionid mussels and their known host fishes from a macroevolutionary perspective to test whether and how ecological and evolutionary factors correlate with patterns of host use. A subset of 69 mussel species was chosen based on data availability regarding their fish host repertoires, phylogenetic relationships, and ecology. Despite the brevity of their parasitic life stages, the mussels conformed to the right-skewed distribution of host specificity typical of parasitic taxa, in which most species are specialists and a few are generalists. Phylogenetic least squares regression models identified affinity for low-gradient and riffle habitats, and colonization of post-glacial watersheds as the best predictors for the number of fish host species per mussel. However, the second-best model identified citation number as a predictor of the number of hosts, implying that many mussel–host interactions still remain to be identified. A Multiple Regression Mantel test was performed to identify factors associated with the proportion of hosts shared between pairs of mussel species. Range overlap, citations, genetic distance, and similarity in host infection strategy were significantly correlated with the proportion of hosts shared, yet total variation as explained by the best model was low (R²?=?0.14). There was evidence of a topological association between mussels and their hosts (P?=?0.001) and a significant phylogenetic signal of host specificity (λ?=?0.81, P?=?0.003), indicating closely related mussels that overlap in range are more likely to be competing for hosts. Our results provide an initial macroevolutionary framework for studying the evolution of host infection strategies in these mussels but also highlights gaps still remaining in our fundamental ecological knowledge of this endangered clade.     

Macroevolution via secondary endosymbiosis: a Neo-Goldschmidtian view of unicellular hopeful monsters and Darwin’s primordial intermediate form

Seventy-five years ago, the geneticist Richard Goldschmidt hypothesized that single mutations affecting development could result in major phenotypic changes in a single generation to produce unique organisms within animal populations that he called “hopeful monsters”. Three decades ago, Sarah P. Gibbs proposed that photosynthetic unicellular micro-organisms like euglenoids and dinoflagellates are the products of a process now called “secondary endosymbiosis” (i.e., the evolution of a chloroplast surrounded by three or four membranes resulting from the incorporation of a eukaryotic alga by a eukaryotic heterotrophic host cell). In this article, we explore the evidence for Goldschmidt’s “hopeful monster” concept and expand the scope of this theory to include the macroevolutionary emergence of organisms like Euglena and Chlorarachnion from secondary endosymbiotic events. We argue that a Neo-Goldschmidtian perspective leads to the conclusion that cell chimeras such as euglenids and dinoflagellates, which are important groups of phytoplankton in freshwater and marine ecosystems, should be interpreted as “successful monsters”. In addition, we argue that Charles Darwin had euglenoids (infusoria) in mind when he speculated on the “primordial intermediate form”, although his Proto-Euglena-hypothesis for the origin of the last common ancestor of all forms of life is no longer acceptable.     

Inferring developmental constraint and constraint release: primordial germ cell determination mechanisms as examples

Developmental constraint and its converse constraint release are significant concepts in understanding pattern and process in macroevolution. The purpose of this paper is to propose a two-step method for identifying constraints and constraint release. The first step is a phylogenetic optimization procedure to identify which trait/process is primitive and which is derived. The primitive trait is inferred to be the constraint and the convergently derived trait the release. The second criterion uses sister-clade asymmetry. Clades diagnosed by the constraint will have fewer taxa than clades diagnosed by the release. As an example, we use the process of germ cell specification, in which there are three modes of specification. Our results corroborate previous conclusions that the induced mode is the constraint and the predetermined mode is the release and we speculate on the importance of these two processes in terms of robustness and evolvability.     

Early tetrapodomorph biogeography: Controlling for fossil record bias in macroevolutionary analyses

The fossil record provides direct empirical data for understanding macroevolutionary patterns and processes. Inherent biases in the fossil record are well known to confound analyses of this data. Sampling bias proxies have been used as covariates in regression models to test for such biases. Proxies, such as formation count, are associated with paleobiodiversity, but are insufficient for explaining species dispersal owing to a lack of geographic context. Here, we develop a sampling bias proxy that incorporates geographic information and test it with a case study on early tetrapodomorph biogeography. We use recently-developed Bayesian phylogeographic models and a new supertree of early tetrapodomorphs to estimate dispersal rates and ancestral habitat locations. We find strong evidence that geographic sampling bias explains supposed radiations in dispersal rate (potential adaptive radiations). Our study highlights the necessity of accounting for geographic sampling bias in macroevolutionary and phylogenetic analyses and provides an approach to test for its effect.     

Not Looking a Gift Horse in the Mouth: Exploring the Merits of a Student–Teacher–Scientist Partnership

One major emphasis of reform initiatives in science education is the importance of extended inquiry experiences for students through authentic collaborations with scientists. As such, unique partnerships have started to emerge between science and education in an ongoing effort to capture the interest and imaginations of students as they make sense of the world around them. One such partnership is called the student–teacher–scientist partnership, in which teachers and their students participate in and contribute to the research of scientists. This article explores a partnership between a 10th-grade biology teacher, her students, and practicing scientists who collaborated in the design, implementation and evaluation of a horse evolution unit. The primary goal of the collaborative activity was to involve teachers and students in a process of conceptual change as a means of eliminating common misconceptions implicit in horse evolution displays in museums in various parts of the country. The evidence-based lessons developed enhanced students’ understanding of concepts in macroevolution but also connected the science classroom with a community of scientists whose personalization of the horse evolution unit situated biological concepts and the learning experience within the context of real-world issues.     

How much can we know about the causes of evolutionary trends?

One of the first questions that paleontologists ask when they identify a large-scale trend in the fossil record (e.g., size increase, complexity increase) is whether it is passive or driven. In this article, I explore two questions about driven trends: (1) what is the underlying cause or source of the directional bias? and (2) has the strength of the directional bias changed over time? I identify two underdetermination problems that prevent scientists from giving complete answers to these two questions.     

THE PENNSYLVANIAN-PERMIAN VEGETATIONAL TRANSITION: A TERRESTRIAL ANALOGUE TO THE ONSHORE-OFFSHORE HYPOTHESIS

An analysis of 68 floras from the Pennsylvanian and Early Permian of Euramerica reveals distinct patterns of environmental distribution. Wetland assemblages are the most commonly encountered floras from the Early and Middle Pennsylvanian. Floras from drier habitats characterize the Permian. Both wetland and dry-site floras occur in the Late Pennsylvanian, but floristic overlap is minimal, which implies strong environmental controls on the distributions of the component species. Drier habitats appear to be the sites of first appearance of orders that become prominent during the Late Permian and Mesozoic. Higher taxa originated in physically heterogeneous, drier habitats, which were geographically marginal throughout most of the Pennsylvanian. They then moved into the lowlands during periods of climatic drying in the Permian, replacing older wetland vegetation. This pattern is analogous to the marine onshore-offshore pattern of origination and migration. The derivation of Mesozoic wetland clades from the Permian dry-lowland vegetation completes the parallel. The similarities of the marine and terrestrial patterns suggest that the combination of evolutionary opportunity, created by physical heterogeneity of the environment, and migrational opportunity, created by changing extrinsic conditions, may be underlying factors that transcend the specifics of organism and environment.