Evolutionary reorganizations of ontogenesis in related species of coenobial volvocine algae

The evolutionary aspects of ontogenesis in green volvocine algae have been considered on the basis of the author’s and published data, as well as the information on taxonomy, phylogeny, and ecology of this group. Analysis of the rate, diurnal rhythm, and light/dark control of cell divisions in various species, as well as experiments with the nucleic acid and protein synthesis inhibitors made it possible to elucidate cellular mechanisms underlying evolutionary rearrangements of asexual development in the genus Volvox.     

Origins of multicellular complexity: Volvox and the volvocine algae

The collection of evolutionary transformations known as the ‘major transitions’ or ‘transitions in individuality’ resulted in changes in the units of evolution and in the hierarchical structure of cellular life. Volvox and related algae have become an important model system for the major transition from unicellular to multicellular life, which touches on several fundamental questions in evolutionary biology. The Third International Volvox Conference was held at the University of Cambridge in August 2015 to discuss recent advances in the biology and evolution of this group of algae. Here, I highlight the benefits of integrating phylogenetic comparative methods and experimental evolution with detailed studies of developmental genetics in a model system with substantial genetic and genomic resources. I summarize recent research on Volvox and its relatives and comment on its implications for the genomic changes underlying major evolutionary transitions, evolution and development of complex traits, evolution of sex and sexes, evolution of cellular differentiation and the biophysics of motility. Finally, I outline challenges and suggest future directions for research into the biology and evolution of the volvocine algae.     

Okasha’s evolution and the levels of selection: toward a broader conception of theoretical biology

The debate about the levels of selection has been one of the most controversial both in evolutionary biology and in philosophy of science. Okasha’s book makes the sort of contribution that simply will not be able to be ignored by anyone interested in this field for many years to come. However, my interest here is in highlighting some examples of how Okasha goes about discussing his material to suggest that his book is part of an increasingly interesting trend that sees scientists and philosophers coming together to build a broadened concept of “theory” through a combination of standard mathematical treatments and conceptual analyses. Given the often contentious history of the relationship between philosophy and science, such trend cannot but be welcome.     

Chloroplast phylogenomics of unicellular and colonial Volvocales provides perspectives on the evolution of morphological characters

Volvocales forms a species-rich clade with wide morphological variety and is regarded as an ideal model for tracing the evolutionary transitions in multicellularity. The phylogenetic relationships among the colonial volvocine algae and its relatives are important for investigating the origin of multicellularity in the clade Reinhardtinia. Therefore, a robust phylogenetic framework of the unicellular and colonial volvocine algae with broad taxon and gene sampling is essential for illuminating the evolution of multicellularity. Recent chloroplast phylogenomic studies have uncovered five major orders in the Chlorophyceae, but the family-level relationships within Sphaeropleales and Volvocales remain elusive due to the uncertain positions of some incertae sedis taxa. In this study, we contributed six newly sequenced chloroplast genomes in the Volvocales and analyzed a dataset with 91 chlorophycean taxa and 58 protein-coding genes. Conflicting phylogenetic signals were detected among chloroplast genes that resulted in discordant tree topologies among different analyses. We compared the phylogenetic trees inferred from original nucleotide, RY-coding, codon-degenerate, and amino acid datasets, and improved the robustness of phylogenetic inference in the Chlorophyceae by reducing base compositional bias. Our analyses indicate that the unicellular Chlamydomonas and Vitreochlamys are close to or nested within the colonial taxa, and all the incertae sedis taxa are nested within the monophyletic Sphaeropleales s.l. We propose that the colonial taxa in the Reinhardtinia are paraphyletic and multicellularity evolved once in the volvocine green algae and might be lost in Chlamydomonas and Vitreochlamys.     

Analysis of mitochondrial and chloroplast genomes in two volvocine algae: Eudorina elegans and Eudorina cylindrica (Volvocaceae,Chlorophyta)

The colonial volvocine algae span the full range of organizational complexity, from four-celled species to multicellular species, and this group of algae is often used for the study of evolution. In recent years, many organelle genomes have been sequenced using the application of next generation sequencing technology; however, only a few organelle genomes have been reported in colonial volvocine algae. In this study, we determined the organelle genomes of Eudorina elegans and Eudorina cylindrica and analysed the organelle genome size, structure and gene content between these volvocine species. This provided useful information to help us understand the composition of colonial volvocine organelle genomes. Based on the chloroplast genome protein-coding genes, we conducted a phylogenomics analysis of the volvocine algae. The result revealed an unexpected phylogenetic relationship, namely, E. elegans is more closely related to Pleodorina starrii than to E. cylindrica. The substitution rate of volvocine algae was then calculated based on organelle genome protein-coding genes; our analysis suggested the possibility that the two Eudorina species may be under similar evolutionary pressure. Lastly, the synteny analysis of the mitochondrial genome showed that gene arrangements and contents are highly conserved in the family Volvocaceae, and the synteny analysis of the chloroplast genome indicated that the genus Eudorina may have experienced genomic changes.     

The Simplest Integrated Multicellular Organism Unveiled

Volvocine green algae represent the “evolutionary time machine” model lineage for studying multicellularity, because they encompass the whole range of evolutionary transition of multicellularity from unicellular Chlamydomonas to >500-celled Volvox. Multicellular volvocalean species including Gonium pectorale and Volvox carteri generally have several common morphological features to survive as integrated multicellular organisms such as “rotational asymmetry of cells” so that the cells become components of the individual and “cytoplasmic bridges between protoplasts in developing embryos” to maintain the species-specific form of the multicellular individual before secretion of new extracellular matrix (ECM). However, these morphological features have not been studied in the four-celled colonial volvocine species Tetrabaena socialis that is positioned in the most basal lineage within the colonial or multicellular volvocine greens. Here we established synchronous cultures of T. socialis and carried out immunofluorescence microscopic and ultrastructural observations to elucidate these two morphological attributes. Based on immunofluorescence microscopy, four cells of the mature T. socialis colony were identical in morphology but had rotational asymmetry in arrangement of microtubular rootlets and separation of basal bodies like G. pectorale and V. carteri. Ultrastructural observations clearly confirmed the presence of cytoplasmic bridges between protoplasts in developing embryos of T. socialis even after the formation of new flagella in each daughter protoplast within the parental ECM. Therefore, these two morphological attributes might have evolved in the common four-celled ancestor of the colonial volvocine algae and contributed to the further increase in cell number and complexity of the multicellular individuals of this model lineage. T. socialis is one of the simplest integrated multicellular organisms in which four identical cells constitute the individual.     

Repeated evolution and reversibility of self‐fertilization in the volvocine green algae*

Outcrossing and self‐fertilization are fundamental strategies of sexual reproduction, each with different evolutionary costs and benefits. Self‐fertilization is thought to be an evolutionary “dead‐end” strategy, beneficial in the short term but costly in the long term, resulting in self‐fertilizing species that occupy only the tips of phylogenetic trees. Here, we use volvocine green algae to investigate the evolution of self‐fertilization. We use ancestral‐state reconstructions to show that self‐fertilization has repeatedly evolved from outcrossing ancestors and that multiple reversals from selfing to outcrossing have occurred. We use three phylogenetic metrics to show that self‐fertilization is not restricted to the tips of the phylogenetic tree, a finding inconsistent with the view of self‐fertilization as a dead‐end strategy. We also find no evidence for higher extinction rates or lower speciation rates in selfing lineages. We find that self‐fertilizing species have significantly larger colonies than outcrossing species, suggesting the benefits of selfing may counteract the costs of increased size. We speculate that our macroevolutionary results on self‐fertilization (i.e., non‐tippy distribution, no decreased diversification rates) may be explained by the haploid‐dominant life cycle that occurs in volvocine algae, which may alter the costs and benefits of selfing.     

EARLY EVOLUTION OF THE GENETIC BASIS FOR SOMA IN THE VOLVOCACEAE

To understand the hierarchy of life in evolutionary terms, we must explain why groups of one kind of individual, say cells, evolve into a new higher level individual, a multicellular organism. A fundamental step in this process is the division of labor into nonreproductive altruistic soma. The regA gene is critical for somatic differentiation in Volvox carteri, a multicellular species of volvocine algae. We report the sequence of regA‐like genes and several syntenic markers from divergent species of Volvox. We show that regA evolved early in the volvocines and predict that lineages with and without soma descended from a regA‐containing ancestor. We hypothesize an alternate evolutionary history of regA than the prevailing “proto‐regA” hypothesis. The variation in presence of soma may be explained by multiple lineages independently evolving soma utilizing regA or alternate genetic pathways. Our prediction that the genetic basis for soma exists in species without somatic cells raises a number of questions, most fundamentally, under what conditions would species with the genetic potential for soma, and hence greater individuality, not evolve these traits. We conclude that the evolution of individuality in the volvocine algae is more complicated and labile than previously appreciated on theoretical grounds.     

Cleavage, incomplete inversion, and cytoplasmic bridges in Gonium pectorale (Volvocales, Chlorophyta)

Multicellularity arose several times in evolution of eukaryotes. The volvocine algae have full range of colonial organization from unicellular to colonies, and thus these algae are well-known models for examining the evolution and mechanisms of multicellularity. Gonium pectorale is a multicellular species of Volvocales and is thought to be one of the first small colonial organisms among the volvocine algae. In these algae, a cytoplasmic bridge is one of the key traits that arose during the evolution of multicellularity. Here, we observed the inversion process and the cytoplasmic bridges in G. pectorale using time-lapse, fluorescence, and electron microscopy. The cytoplasmic bridges were located in the middle region of the cell in 2-, 4-, 8-, and 16-celled stages and in inversion stages. However, there were no cytoplasmic bridges in the mature adult stage. Cytoplasmic bridges and cortical microtubules in G. pectorale suggest that a mechanism of kinesin-microtubule machinery similar to that in other volvocine algae is responsible for inversion in this species.     

Ontogenetic diversity of colonies and intercellular cytoplasmic bridges in the algae of the genus Volvox

In all representatives of the genus Volvox, cells of cleaving embryos are connected by cytoplasmic bridges, which play an important role in the process of young colony inversion. However, during subsequent development, the intercellular bridges are retained not in all species of Volvox; the occurrence of the bridges in an adult colony correlates with the small size of mature gonidia (asexual reproductive cells) and with the presence of cell growth in the intervals between divisions. This complex of ontogenetic features is derived and arises independently in three evolutionary lineages of colonial volvocine algae. A putative role of the syncytial state of adult colonies for the evolution of developmental cycles in Volvox is discussed.     

Samir Okasha: Evolution and the levels of selection

The debate about the levels of selection has been one of the most controversial both in evolutionary biology and in philosophy of science. Okasha’s book makes the sort of contribution that simply will not be able to be ignored by anyone interested in this field for many years to come. However, my interest here is in highlighting some examples of how Okasha goes about discussing his material to suggest that his book is part of an increasingly interesting trend that sees scientists and philosophers coming together to build a broadened concept of “theory” through a combination of standard mathematical treatments and conceptual analyses. Given the often contentious history of the relationship between philosophy and science, such trend cannot but be welcome.     

Genetic differentiation and limited gene flow among fragmented populations of New Zealand endemic Hector’s and Maui’s dolphins

Gene flow among small fragmented populations is critical for maintaining genetic diversity, and therefore the evolutionary potential of a species. Concern for two New Zealand endemic subspecies, the Hector’s (Cephalorhynchus hectori hectori) and Maui’s (C. h. maui) dolphins, arises from their low abundance, slow rate of reproduction, and susceptibility to fisheries-related mortality. Our work examined genetic differentiation and migration between the subspecies and among regional and local Hector’s dolphin populations using mitochondrial (mt) DNA and microsatellite genotypes from 438 samples. Results confirmed earlier reports of a single unique mtDNA control region haplotype fixed in the Maui’s dolphin, and provided new evidence of reproductive isolation from Hector’s dolphins (9-locus microsatellite F _ST?=?0.167, P?<?0.001). Independent evolutionary trajectories were also supported for Hector’s dolphin populations of the East Coast, West Coast, Te Waewae Bay and Toetoe Bay. Low asymmetrical migration rates were found among several Hector’s dolphin populations and assignment tests identified five Hector’s dolphins likely to have a migrant father from another regional population. There appears to be sufficient step-wise gene flow to maintain genetic diversity within the East and West Coasts; however, the two local South Coast populations exhibited a high degree of differentiation given their close proximity (~100?km). To maintain the evolutionary potential and long-term survival of both subspecies, genetic monitoring and conservation management must focus on maintaining corridors to preserve gene flow and prevent further population fragmentation and loss of genetic diversity, in addition to maintaining local population abundances.     

Diet and hormonal manipulation reveal cryptic genetic variation: implications for the evolution of novel feeding strategies

When experiencing resource competition or abrupt environmental change, animals often must transition rapidly from an ancestral diet to a novel, derived diet. Yet, little is known about the proximate mechanisms that mediate such rapid evolutionary transitions. Here, we investigated the role of diet-induced, cryptic genetic variation in facilitating the evolution of novel resource-use traits that are associated with a new feeding strategy—carnivory—in tadpoles of spadefoot toads (genus Spea). We specifically asked whether such variation in trophic morphology and fitness is present in Scaphiopus couchii, a species that serves as a proxy for ancestral Spea. We also asked whether corticosterone, a vertebrate hormone produced in response to environmental signals, mediates the expression of this variation. Specifically, we compared broad-sense heritabilities of tadpoles fed different diets or treated with exogenous corticosterone, and found that novel diets can expose cryptic genetic variation to selection, and that diet-induced hormones may play a role in revealing this variation. Our results therefore suggest that cryptic genetic variation may have enabled the evolutionary transition to carnivory in Spea tadpoles, and that such variation might generally facilitate rapid evolutionary transitions to novel diets.     

More on how and why: cause and effect in biology revisited

In 1961, Ernst Mayr published a highly influential article on the nature of causation in biology, in which he distinguished between proximate and ultimate causes. Mayr argued that proximate causes (e.g. physiological factors) and ultimate causes (e.g. natural selection) addressed distinct ‘how’ and ‘why’ questions and were not competing alternatives. That distinction retains explanatory value today. However, the adoption of Mayr’s heuristic led to the widespread belief that ontogenetic processes are irrelevant to evolutionary questions, a belief that has (1) hindered progress within evolutionary biology, (2) forged divisions between evolutionary biology and adjacent disciplines and (3) obstructed several contemporary debates in biology. Here we expand on our earlier (Laland et al. in Science 334:1512–1516, 2011) argument that Mayr’s dichotomous formulation has now run its useful course, and that evolutionary biology would be better served by a concept of reciprocal causation, in which causation is perceived to cycle through biological systems recursively. We further suggest that a newer evolutionary synthesis is unlikely to emerge without this change in thinking about causation.     

Maynard Smith,optimization, and evolution

Maynard Smith’s defenses of adaptationism and of the value of optimization theory in evolutionary biology are both criticized. His defense does not adequately respond to the criticism of adaptationism by Gould and Lewontin. It is also argued here that natural selection cannot be interpreted as an optimization process if the objective function to be optimized is either (i) interpretable as a fitness, or (ii) correlated with the mean population fitness. This result holds even if fitnesses are frequency-independent; the problem is further exacerbated in the frequency-dependent context modeled by evolutionary game theory. However, Eshel and Feldman’s new results on “long-term” evolution may provide some hope for the continuing relevance of the game-theoretic framework. These arguments also demonstrate the irrelevance of attempts by Intelligent Design creationists to use computational limits on optimization algorithms as evidence against evolutionary theory. It is pointed out that adaptation, natural selection, and optimization are not equivalent processes in the context of biological evolution. It is a pleasure to dedicate this paper to the memory of John Maynard Smith. Thanks are due to James Justus and Samir Okasha for comments on an earlier draft.     

The measurement of coevolution in the wild

Coevolution has long been thought to drive the exaggeration of traits, promote major evolutionary transitions such as the evolution of sexual reproduction and influence epidemiological dynamics. Despite coevolution’s long suspected importance, we have yet to develop a quantitative understanding of its strength and prevalence because we lack generally applicable statistical methods that yield numerical estimates for coevolution’s strength and significance in the wild. Here, we develop a novel method that derives maximum likelihood estimates for the strength of direct pairwise coevolution by coupling a well‐established coevolutionary model to spatially structured phenotypic data. Applying our method to two well‐studied interactions reveals evidence for coevolution in both systems. Broad application of this approach has the potential to further resolve long‐standing evolutionary debates such as the role species interactions play in the evolution of sexual reproduction and the organisation of ecological communities.     

Major problems in evolutionary transitions: how a metabolic perspective can enrich our understanding of macroevolution

The model of major transitions in evolution (MTE) devised by Maynard Smith and Szathmáry has exerted tremendous influence over evolutionary theorists. Although MTE has been criticized for inconsistently combining different types of event, its ongoing appeal lies in depicting hierarchical increases in complexity by means of evolutionary transitions in individuality (ETIs). In this paper, we consider the implications of major evolutionary events overlooked by MTE and its ETI-oriented successors, specifically the biological oxygenation of Earth, and the acquisitions of mitochondria and plastids. By reflecting on these missed events, we reveal a central philosophical disagreement over the explanatory goals of major transitions theory that has yet to be made explicit in the literature. We go on to argue that this philosophical disagreement is only reinforced by Szathmáry’s recent revisions of MTE in the form of MTE 2.0. This finding motivates us to propose an alternative explanatory strategy: specifically, an interactionist metabolic perspective on major transitions. A metabolic framework not only avoids many of the criticisms that beset classic and revised MTE models, but also accommodates missing events and provides crucial explanatory components for standard major transitions. Although we do not provide a full-blown alternative theory and do not claim to achieve unity, we explain why foregrounding metabolism is crucial for any attempt to capture the major turning points in evolution, and why it does not lead to unmanageable pluralism.     

The Impact of Lamarck’s Theory of Evolution Before Darwin’s Theory

This paper analyzes the impact that Lamarckian evolutionary theory had in the scientific community during the period between the advent of Zoological Philosophy and the publication Origin of Species. During these 50 years Lamarck’s model was a well known theory and it was discussed by the scientific community as a hypothesis to explain the changing nature of the fossil record throughout the history of Earth. Lamarck’s transmutation theory established the foundation of an evolutionary model introducing a new way to research in nature. Darwin’s selectionist theory was proposed in 1859 to explain the origin of species within this epistemological process. In this context, Charles Lyell’s Principles of Geology and Auguste Comte’s Cours de Philosophie Positive appear as two major works for the dissemination of Lamarck’s evolutionary ideology after the death of the French naturalist in 1829.