Phylogeny and molecular evolution of the green algae

Co-authored with Frederik Leliaert, David R. Smith, Hervé Moreau, Heroen Verbruggen, Charles F. Delwiche, and Olivier De Clerck,

The green lineage (Viridiplantae) comprises the green algae and their descendants the land plants, and is one of the major groups of oxygenic photosynthetic eukaryotes. Current hypotheses posit the early divergence of two discrete clades from an ancestral green flagellate. One clade, the Chlorophyta, comprises the early diverging prasinophytes, which gave rise to the core chlorophytes. The other clade, the Streptophyta, includes the charophyte green algae from which the land plants evolved. Multi-marker and genome scale phylogenetic studies have greatly improved our understanding of broad-scale relationships of the green lineage, yet many questions persist, including the branching orders of the prasinophyte lineages, the relationships among core chlorophyte clades (Chlorodendrophyceae, Ulvophyceae, Trebouxiophyceae and Chlorophyceae), and the relationships among the streptophytes. Current phylogenetic hypotheses provide an evolutionary framework for molecular evolutionary studies and comparative genomics. This review summarizes our current understanding of organelle genome evolution in the green algae, genomic insights into the ecology of oceanic picoplanktonic prasinophytes, molecular mechanisms underlying the evolution of complexity in volvocine green algae, and the evolution of genetic codes and the translational apparatus in green seaweeds. Finally, we discuss molecular evolution in the streptophyte lineage, emphasizing the genetic facilitation of land plant origins.

Adaptive diversification of a plastic trait in a predictably fluctuating environment

Co-authored with Michael Doebeli

There is substantial evidence that evolutionary diversification can occur in allopatric conditions through reduction in the degree of phenotypic plasticity when an isolated population encounters a novel, more stable environment. Plasticity is no longer favored in the new environment, either because it carries an inherent physiological cost or because it leads to production of suboptimal phenotypes. In order to explore the role of phenotypic plasticity in sympatric diversification, we modeled the ecological and evolutionary dynamics of Escherichia coli bacteria in batch cultures. Our results describe an evolutionary pathway leading to metabolic diversification in a sympatric environment without spatial structure. In an environment that fluctuates widely and predictably, evolutionary branching leads to diversification and stable coexistence of generalist and specialist ecotypes for some combinations of parameters. Diversification and stable coexistence occur when reaction norms are steep and trade-offs between metabolic pathways are convex. We conclude that, in principle, diversification due to reduced plasticity can occur without allopatric isolation, reduced environmental variability, or an explicit cost of plasticity.

On the paradigm of altruistic suicide in the unicellular world

Co-authored with A. M. Nedelcu, W. W. Driscoll, P. M. Durand, and A. Rashidi; published in Evolution.

Altruistic suicide is best known in the context of programmed cell death (PCD) in multicellular individuals, which is understood as an adaptive process that contributes to the development and functionality of the organism. After the realization that PCD-like processes can also be induced in single-celled lineages, the paradigm of altruistic cell death has been extended to include these active cell death processes in unicellular organisms. Here, we critically evaluate the current conceptual framework and the experimental data used to support the notion of altruistic suicide in unicellular lineages, and propose new perspectives. We argue that importing the paradigm of altruistic cell death from multicellular organisms to explain active death in unicellular lineages has the potential to limit the types of questions we ask, thus biasing our understanding of the nature, origin, and maintenance of this trait. We also emphasize the need to distinguish between the benefits and the adaptive role of a trait. Lastly, we provide an alternative framework that allows for the possibility that active death in single-celled organisms is a maladaptive trait maintained as a byproduct of selection on pro-survival functions, but that could—under conditions in which kin/group selection can act—be co-opted into an altruistic trait.

Evolution of developmental programs in Volvox (Chlorophyta)

Co-authored with A. E. Desnitskiy and R. E. Michod

The volvocine green algal genus Volvox includes ∼20 species with diverse sizes (in terms of both diameter and cell number), morphologies, and developmental programs. Two suites of characters are shared among distantly related lineages within Volvox. The traits characteristic of all species of Volvox—large (>500) numbers of small somatic cells, much smaller numbers of reproductive cells, and oogamy in sexual reproduction—have three or possibly four separate origins. In addition, some species have evolved a suite of developmental characters that differs from the ancestral developmental program. Most multicellular volvocine algae, including some species of Volvox, share an unusual pattern of cell division known as palintomy or multiple fission. Asexual reproductive cells (gonidia) grow up to many times their initial size and then divide several times in rapid succession, with little or no growth between divisions. Three separate Volvox lineages have evolved a reduced form of palintomy in which reproductive cells are small and grow between cell divisions. In each case, these changes are accompanied by a reduction in the rate of cell division and by a requirement of light for cell division to occur. Thus, two suites of characters—those characteristic of all Volvox species and those related to reduced palintomy—have each evolved convergently or in parallel in lineages that diverged at least 175 million years ago (mya).

Many from one: lessons from the volvocine algae on the evolution of multicellularity

The volvocine green algae are a model system for the evolution of multicellularity and cellular differentiation. A combination of molecular genetic and phylogenetic comparative approaches has resulted in a detailed picture of the transition from single cells to differentiated, multicellular organisms in this group. To be useful as a model system, the volvocine algae should provide information that is relevant to other groups. Here I discuss recent advances in understanding the origins of multicellularity and cellular differentiation in the volvocine algae and consider the implications for such transitions in general. Several general principles emerge that are relevant to the origins of major multicellular groups, such as animals, plants, fungi, and red and brown algae. First, if the lessons learned from the volvocine algae can be generalized to other origins of multicellularity, we should expect these transitions to be understandable as a series of small changes, each potentially adaptive in itself. In addition, cooperation, conflict and mediation of conflicts among cells are likely to have played central roles. Finally, we should expect the histories of these transitions to include parallel evolution of some traits, periods of relatively rapid change interspersed with long periods of stasis, and simpler forms coexisting with more complex forms for long periods of time as in the evolution of the volvocine algae.

Triassic origin and early radiation of multicellular volvocine algae

Co-authored with J. D. Hackett, F. O. Aylward, and R. E. Michod.

Evolutionary transitions in individuality (ETIs) underlie the watershed events in the history of life on Earth, including the origins of cells, eukaryotes, plants, animals, and fungi. Each of these events constitutes an increase in the level of complexity, as groups of individuals become individuals in their own right. Among the best-studied ETIs is the origin of multicellularity in the green alga Volvox, a model system for the evolution of multicellularity and cellular differentiation. Since its divergence from unicellular ancestors, Volvox has evolved into a highly integrated multicellular organism with cellular specialization, a complex developmental program, and a high degree of coordination among cells. Remarkably, all of these changes were previously thought to have occurred in the last 50–75 million years. Here we estimate divergence times using a multigene data set with multiple fossil calibrations and use these estimates to infer the times of developmental changes relevant to the evolution of multicellularity. Our results show that Volvox diverged from unicellular ancestors at least 200 million years ago. Two key innovations resulting from an early cycle of cooperation, conflict and conflict mediation led to a rapid integration and radiation of multicellular forms in this group. This is the only ETI for which a detailed timeline has been established, but multilevel selection theory predicts that similar changes must have occurred during other ETIs.

Does biology need an organism concept?

Co-authored with J. W. Pepper

Among biologists, there is no general agreement on exactly what entities qualify as ‘organisms’. Instead, there are multiple competing organism concepts and definitions. While some authors think this is a problem that should be corrected, others have suggested that biology does not actually need an organism concept. We argue that the organism concept is central to biology and should not be abandoned. Both organism concepts and operational definitions are useful. We review criteria used for recognizing organisms and conclude that they are not categorical but rather continuously variable. Different organism concepts are useful for addressing different questions, and it is important to be explicit about which is being used. Finally, we examine the origins of the derived state of organismality, and suggest that it may result from positive feedback between natural selection and functional integration in biological entities.

Evolution of complexity in the volvocine algae: transitions in individuality through Darwin's eye

Co-authored with R. E. Michod

The transition from unicellular to differentiated multicellular organisms constitutes an increase in the level complexity, because previously existing individuals are combined to form a new, higher-level individual. The volvocine algae represent a unique opportunity to study this transition because they diverged relatively recently from unicellular relatives and because extant species display a range of intermediate grades between unicellular and multicellular, with functional specialization of cells. Following the approach Darwin used to understand "organs of extreme perfection" such as the vertebrate eye, this jump in complexity can be reduced to a series of small steps that cumulatively describe a gradual transition between the two levels. We use phylogenetic reconstructions of ancestral character states to trace the evolution of steps involved in this transition in volvocine algae. The history of these characters includes several well-supported instances of multiple origins and reversals. The inferred changes can be understood as components of cooperation–conflict–conflict mediation cycles as predicted by multilevel selection theory. One such cycle may have taken place early in volvocine evolution, leading to the highly integrated colonies seen in extant volvocine algae. A second cycle, in which the defection of somatic cells must be prevented, may still be in progress.

Comparative mitochondrial genomics of snakes: substitution rate dynamics and functionality of the duplicate control region

Co-authored with Jiang, Z. J., T. A. Castoe, C. C. Austin, F. T. Burbrink, J. A. McGuire, C. L. Parkinson, and D. D. Pollock

Background

The mitochondrial genomes of snakes are characterized by an overall evolutionary rate that appears to be one of the most accelerated among vertebrates. They also possess other unusual features, including short tRNAs and other genes, and a duplicated control region that has been stably maintained since it originated more than 70 million years ago. Here, we provide a detailed analysis of evolutionary dynamics in snake mitochondrial genomes to better understand the basis of these extreme characteristics, and to explore the relationship between mitochondrial genome molecular evolution, genome architecture, and molecular function. We sequenced complete mitochondrial genomes from Slowinski's corn snake (Pantherophis slowinskii) and two cottonmouths (Agkistrodon piscivorus) to complement previously existing mitochondrial genomes, and to provide an improved comparative view of how genome architecture affects molecular evolution at contrasting levels of divergence.
Results

We present a Bayesian genetic approach that suggests that the duplicated control region can function as an additional origin of heavy strand replication. The two control regions also appear to have different intra-specific versus inter-specific evolutionary dynamics that may be associated with complex modes of concerted evolution. We find that different genomic regions have experienced substantial accelerated evolution along early branches in snakes, with different genes having experienced dramatic accelerations along specific branches. Some of these accelerations appear to coincide with, or subsequent to, the shortening of various mitochondrial genes and the duplication of the control region and flanking tRNAs.
Conclusion

Fluctuations in the strength and pattern of selection during snake evolution have had widely varying gene-specific effects on substitution rates, and these rate accelerations may have been functionally related to unusual changes in genomic architecture. The among-lineage and among-gene variation in rate dynamics observed in snakes is the most extreme thus far observed in animal genomes, and provides an important study system for further evaluating the biochemical and physiological basis of evolutionary pressures in vertebrate mitochondria.

Cooperation and conflict during evolutionary transitions in individuality

Co-authored with R. E. Michod

Cooperation received much less attention 30 years ago than other forms of ecological interaction, such as competition and predation. Workers generally viewed cooperation as being of limited interest, of special relevance to certain species (e.g. social insects, birds, humans and our primate relatives) but not of general significance to life on earth. This view has changed, due in large part to the study of evolutionary transitions in individuality (ETIs). What began as the study of animal social behaviour some 40 years ago has now embraced the study of social interactions at all levels in the hierarchy of life. Instead of being seen as a special characteristic clustered in certain lineages of social animals, cooperation is now seen as the primary creative force behind ever greater levels of complexity through the creation of new kinds of individuals. Cooperation plays this central role in ETIs because it exports fitness from the lower level (its costs) to the new higher level (its benefits).

Phylogeny and historical biogeography of African ground squirrels: the role of climate change in the evolution of Xerus

Co-authored with J. M. Waterman and C. L. Parkinson

We used phylogenetic and phylogeographical methods to infer relationships among African ground squirrels of the genus Xerus. Using Bayesian, maximum-parsimony, nested clade and coalescent analyses of cytochrome b sequences, we inferred interspecific relationships, evaluated the specific distinctness of Cape (Xerus inauris) and mountain (Xerus princeps) ground squirrels, and tested hypotheses for historical patterns of gene flow within X. inauris. The inferred phylogeny supports the hypothesized existence of an 'arid corridor' from the Horn of Africa to the Cape region. Although doubts have been raised regarding the specific distinctness of X. inauris and X. princeps, our analyses show that each represents a distinct well-supported, monophyletic lineage. Xerus inauris includes three major clades, two of which are geographically restricted. The distributions of X. inauris populations are concordant with divergences within and disjunctions between other taxa, which have been interpreted as results of Plio–Pleistocene climate cycles. Nested clade analysis, coalescent analyses, and analyses of genetic structure support allopatric fragmentation as the cause of the deep divergences within this species.

Sciurid phylogeny and the paraphyly of Holarctic ground squirrels (Spermophilus)

Co-authored with T. A. Castoe and C. L. Parkinson

The squirrel family, Sciuridae, is one of the largest and most widely dispersed families of mammals. In spite of the wide distribution and conspicuousness of this group, phylogenetic relationships remain poorly understood. We used DNA sequence data from the mitochondrial cytochrome b gene of 114 species in 21 genera to infer phylogenetic relationships among sciurids based on maximum parsimony and Bayesian phylogenetic methods. Although we evaluated more complex alternative models of nucleotide substitution to reconstruct Bayesian phylogenies, none provided a better fit to the data than the GTR + G + I model. We used the reconstructed phylogenies to evaluate the current taxonomy of the Sciuridae. At essentially all levels of relationships, we found the phylogeny of squirrels to be in substantial conflict with the current taxonomy. At the highest level, the flying squirrels do not represent a basal divergence, and the current division of Sciuridae into two subfamilies is therefore not phylogenetically informative. At the tribal level, the Neotropical pygmy squirrel, Sciurillus, represents a basal divergence and is not closely related to the other members of the tribe Sciurini. At the genus level, the sciurine genus Sciurus is paraphyletic with respect to the dwarf squirrels (Microsciurus), and the Holarctic ground squirrels (Spermophilus) are paraphyletic with respect to antelope squirrels (Ammospermophilus), prairie dogs (Cynomys), and marmots (Marmota). Finally, several species of chipmunks and Holarctic ground squirrels do not appear monophyletic, indicating a need for reevaluation of alpha taxonomy.

Xerus erythropus

Co-authored with J. M. Waterman

Xerus princeps

Co-authored with J. M. Waterman