Matthew D. Herron

Phylogeny and molecular evolution of the green algae

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.

Triassic origin and early radiation of multicellular volvocine algae

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.

Parallel evolutionary dynamics of adaptive diversification in Escherichia coli.

The divergence of Escherichia coli bacteria into metabolically distinct ecotypes has a similar genetic basis and similar evolutionary dynamics across independently evolved populations.

EVOLUTION OF COMPLEXITY IN THE VOLVOCINE ALGAE: TRANSITIONS IN INDIVIDUALITY THROUGH DARWIN'S EYE

Abstract 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.

On the paradigm of altruistic suicide in the unicellular world

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.

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

BackgroundThe 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 Slowinskis 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.ResultsWe 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.ConclusionFluctuations 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.

Experimental evolution of an alternating uni- and multicellular life cycle in Chlamydomonas reinhardtii

The transition to multicellularity enabled the evolution of large, complex organisms, but early steps in this transition remain poorly understood. Here we show that multicellular complexity, including development from a single cell, can evolve rapidly in a unicellular organism that has never had a multicellular ancestor. We subject the alga Chlamydomonas reinhardtii to conditions that favour multicellularity, resulting in the evolution of a multicellular life cycle in which clusters reproduce via motile unicellular propagules. While a single-cell genetic bottleneck during ontogeny is widely regarded as an adaptation to limit among-cell conflict, its appearance very early in this transition suggests that it did not evolve for this purpose. Instead, we find that unicellular propagules are adaptive even in the absence of intercellular conflict, maximizing cluster-level fecundity. These results demonstrate that the unicellular bottleneck, a trait essential for evolving multicellular complexity, can arise rapidly via co-option of the ancestral unicellular form.

Does biology need an organism concept

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.

Cooperation and conflict during evolutionary transitions in individuality.

Cooperation received much less attention 30 years agothan other forms of ecological interaction, such ascompetition and predation. Workers generally viewedcooperation as being of limited interest, of specialrelevance to certain species (e.g. social insects, birds,humans and our primate relatives) but not of generalsignificance to life on earth. This view has changed, duein large part to the study of evolutionary transitions inindividuality (ETIs). What began as the study of animalsocial behaviour some 40 years ago has now embracedthe study of social interactions at all levels in thehierarchy of life. Instead of being seen as a specialcharacteristic clustered in certain lineages of socialanimals, cooperation is now seen as the primary creativeforce behind ever greater levels of complexity throughthe creation of new kinds of individuals. Cooperationplays this central role in ETIs because it exports fitnessfrom the lower level (its costs) to the new higher level (itsbenefits).How did this shift in understanding the importance ofcooperation come about? Darwin (1859), Wilson (1975)and Hamilton (1963, 1964a,b) all understood the import-ance of cooperation for social organisms. There waspioneering work done as early as 1902 on the importanceof cooperation in the struggle for existence (Kropotkin,1902), and there was the now widely accepted theory ofMargulis (1970, 1981) and others on the endosymbioticorigins of mitochondria and chloroplasts in the eukary-otic cell. However, cooperation was also viewed as adestabilizing force in ecological communities and likely oflimited significance because of the positive feedbackloops it creates (May, 1973). Sociobiology had definedaltruism as its core problem (Wilson, 1975), but thealtruism problem was not viewed as general to life onearth until workers began applying cooperation thinkingto the evolution of interactions at other levels in thehierarchy of life in addition to social organisms, such asto the level of genes within gene groups (e.g. Eigen SPrice, 1970, 1972; e.g. Hamilton, 1975; Wade, 1978;Wilson, 1980). The evolutionary transitions problem(Maynard Smith, 1988, 1991; Maynard Smith & Szathm-a´ry, 1995) grew out of these two developments which, ineffect, extended the sociobiology revolution to all kindsof replicating units in the hierarchy of life.Lehmann & Keller (2006) propose a four-way classi-fication scheme for population models of the evolution ofcooperation, according to the issue of whether thebenefits are direct (individual selection) or indirect (kinselection). Within the first category of direct benefits, adistinction is made according to whether the benefits aremediated through the behaviour of another individual(as through learning in reciprocation) or not. Within thesecond category of kin-selected indirect effects, a distinc-tion is made as to whether there are many genesinvolved in the traits or a few (as in the ‘green-beard’effect).The distinction between direct and indirect effects iswidely used to describe social behaviour and the evolu-tionoffitnesseffects associated withinteractions betweenindividuals. This distinction seems less helpful, however,when one’s interest concerns the origin of the individualsthemselves, i.e. ETIs. Indeed the direct-indirect distinc-tion presumes that one knows what the individual is.Direct or indirect with regard to what? The individual,of course.Transforming our understanding of life is the realiza-tion that evolution occurs not only through evolutionwithin populations but also during ETIs – when groupsbecome so integrated they evolve into a new higher-levelindividual. The major landmarks in the diversification oflife and the hierarchical organization of the living worldare consequences of a series of ETIs: from nonlife to life,from networks of cooperating genes to the first prokary-otic-like cell, from prokaryotic to eukaryotic cells, fromunicellular to multicellular organisms, from asexual tosexual populations, and from solitary to social organisms.It is a major challenge to understand why (environmen-tal selective pressures) and how (underlying genetics,physiology and development) the basic features of anevolutionary individual, such as fitness heritability,indivisibility, and evolvability, shift their reference fromthe old to the new level. Classifying the many factorsinvolved in the evolution of cooperation into a fewgeneral categories as Lehmann & Keller (2006) havedone will certainly help in meeting this challenge.Individuals often associate in groups, and under certainconditions these groups evolve into a new kind ofindividual. Cooperation is fundamental to this processbecause it transfers fitness from the lower-level indivi-duals (in terms of its costs) up to the level of the group(the benefits of cooperation), thereby serving to create anew level of fitness and possibly, under certain condi-tions, a new higher-level individual (Michod, 1999).Indeed, as already mentioned, the major levels in thehierarchy of life (genes, gene networks, cells, eukaryoticcells, multicellular organisms) are thought to haveevolved from this process of individuation of groups(Maynard Smith & Szathma´ry, 1995; Michod, 1999).

Cellular differentiation and individuality in the ‘minor’ multicellular taxa

Biology needs a concept of individuality in order to distinguish organisms from parts of organisms and from groups of organisms, to count individuals and compare traits across taxa, and to distinguish growth from reproduction. Most of the proposed criteria for individuality were designed for ‘unitary’ or ‘paradigm’ organisms: contiguous, functionally and physiologically integrated, obligately sexually reproducing multicellular organisms with a germ line sequestered early in development. However, the vast majority of the diversity of life on Earth does not conform to all of these criteria. We consider the issue of individuality in the ‘minor’ multicellular taxa, which collectively span a large portion of the eukaryotic tree of life, reviewing their general features and focusing on a model species for each group. When the criteria designed for unitary organisms are applied to other groups, they often give conflicting answers or no answer at all to the question of whether or not a given unit is an individual. Complex life cycles, intimate bacterial symbioses, aggregative development, and strange genetic features complicate the picture. The great age of some of the groups considered shows that ‘intermediate’ forms, those with some but not all of the traits traditionally associated with individuality, cannot reasonably be considered ephemeral or assumed transitional. We discuss a handful of recent attempts to reconcile the many proposed criteria for individuality and to provide criteria that can be applied across all the domains of life. Finally, we argue that individuality should be defined without reference to any particular taxon and that understanding the emergence of new kinds of individuals requires recognizing individuality as a matter of degree.