Evolution of reproductive development in the volvocine algae

The evolution of multicellularity, the separation of germline cells from sterile somatic cells, and the generation of a male–female dichotomy are certainly among the greatest innovations of eukaryotes. Remarkably, phylogenetic analysis suggests that the shift from simple to complex, differentiated multicellularity was not a unique progression in the evolution of life, but in fact a quite frequent event. The spheroidal green alga Volvox and its close relatives, the volvocine algae, span the full range of organizational complexity, from unicellular and colonial genera to multicellular genera with a full germ–soma division of labor and male–female dichotomy; thus, these algae are ideal model organisms for addressing fundamental issues related to the transition to multicellularity and for discovering universal rules that characterize this transition. Of all living species, Volvox carteri represents the simplest version of an immortal germline producing specialized somatic cells. This cellular specialization involved the emergence of mortality and the production of the first dead ancestors in the evolution of this lineage. Volvocine algae therefore exemplify the evolution of cellular cooperation from cellular autonomy. They also serve as a prime example of the evolution of complex traits by a few successive, small steps. Thus, we learn from volvocine algae that the evolutionary transition to complex, multicellular life is probably much easier to achieve than is commonly believed.     

The nematode Pristionchus pacificus as a model system for integrative studies in evolutionary biology

Comprehensive studies of evolution have historically been hampered by the division among disciplines. Now, as biology moves towards an ‘‐omics’ era, it is more important than ever to tackle the evolution of function and form by considering all those research areas involved in the regulation of phenotypes. Here, we review recent attempts to establish the nematode Pristionchus pacificus as a model organism that allows integrative studies of development and evo‐devo, with ecology and population genetics. Originally developed for comparative study with the nematode Caenorhabditis elegans, P. pacificus provided insight into developmental pathways including dauer formation, vulva and gonad development, chemosensation, innate immunity and neurobiology. Its subsequent discovery across a wide geographic distribution in association with scarab beetles enabled its evaluation in a biogeographic context. Development of an evolutionary field station on La Réunion Island, where P. pacificus is present in high abundance across a number of widespread habitat types, allows examination of the microfacets of evolution – processes of natural selection, adaptation and drift among populations can now be examined in this island setting. The combination of laboratory‐based functional studies with fieldwork in P. pacificus has the long‐term prospective to provide both proximate (mechanistic) and ultimate (evolutionary and ecological) causation and might therefore help to overcome the long‐term divide between major areas in biology.     

Alternation of generations – unravelling the underlying molecular mechanism of a 165‐year‐old botanical observation

Characteristically, land plants exhibit a life cycle with an ‘alternation of generations’ and thus alternate between a haploid gametophyte and a diploid sporophyte. At meiosis and fertilisation the transitions between these two ontogenies take place in distinct single stem cells. The evolutionary invention of an embryo, and thus an upright multicellular sporophyte, in the ancestor of land plants formed the basis for the evolution of increasingly complex plant morphologies shaping Earth's ecosystems. Recent research employing the moss Physcomitrella patens revealed the homeotic gene BELL1 as a master regulator of the gametophyte‐to‐sporophyte transition. Here, we discuss these findings in the context of classical botanical observations.     

Genomic studies on the nature of species: adaptation and speciation in Mimulus

Evolutionary biology is in an exciting era, in which powerful genomic tools make the answers accessible to long‐standing questions about variation, adaptation and speciation. The availability of a suite of genomic resources, a shared knowledge base and a long history of study have made the phenotypically diverse plant genus Mimulus an important system for understanding ecological and evolutionary processes. An international Mimulus Research Meeting was held at Duke University in June 2014 to discuss developments in ecological and evolutionary genetic studies in Mimulus. Here, we report major recent discoveries presented at the meeting that use genomic approaches to advance our understanding of three major themes: the parallel genetic basis of adaptation; the ecological genomics of speciation; and the evolutionary significance of structural genetic variation. We also suggest future research directions for studies of Mimulus and highlight challenges faced when developing new ecological and evolutionary model systems.     

Palaeontology and Evolutionary Developmental Biology: A Science of the Nineteenth and Twenty–first Centuries

A wind of change has swept through palaeontology in the past few decades. Contrast Sir Peter Medawar’s dismissive: ‘palaeontology is a particularly undemanding branch of science’ (as recalled by John Maynard Smith in Sabbagh 1999, p. 158) with ‘Palaeontology: grasping the opportunities in the science of the twenty–first century’, the title of a contribution to a special issue of Geobios by the Cambridge palaeontologist, Simon Conway Morris (1998a). The winds of change have come partly from palaeontologists seeking to broaden the impact of their studies and partly from biologists (neontologists) realizing the contributions that palaeontology can make to their disciplines. Consequently, impressions of past life preserved in stone are coming alive. Fossils are being described and analyzed using new tools and languages as the static fossil record becomes a record of transitions in patterns that can be explained and related to biological, ecological, climatic and tectonic changes. The latest addition is evolutionary developmental biology, or ‘evo–devo’, whose language provides a new basis upon which to interpret anatomical change, both materially and mechanistically. In this review I examine the major contributions made by palaeontology, how palaeontology has been linked to evolution and to embryology in the past, and how links with evo–devo have enlivened and will continue to enliven both palaeontology and evo–devo. Closer links between the two fields should illuminate important unresolved issues related to the origin of the metazoans (e.g. Why is there a conflict between molecular clocks and the fossil record in timing the metazoan radiation; were Precambrian metazoan ancestors similar to extant larvae or to miniature adults?) and to diversification of the metazoans (e.g. How do developmental constraints bias the direction of evolution; how do microevolutionary developmental processes relate to macroevolutionary changes?).     

Chlorella variabilis and Micractinium reisseri sp. nov. (Chlorellaceae,Trebouxiophyceae): Redescription of the endosymbiotic green algae of Paramecium bursaria (Peniculia,Oligohymenophorea) in the 120th year

Symbiotic algae of the ciliate Paramecium bursaria (Ehrenberg) Focker are key species in the fields of virology and molecular evolutionary biology as well as in the biology of symbiotic relationships. These symbiotic algae were once identified as Zoochlorella conductrix Brandt by the Dutch microbiologist, Beijerinck 120 years ago. However, after many twists and turns, the algae are today treated as nameless organisms. Recent molecular analyses have revealed several different algal partners depending on P. bursaria strains, but nearly all P. bursaria contains a symbiont belonging to either the so‐called ‘American’ or ‘European’ group. The absence of proper names for these algae is beginning to provoke ill effects in the above‐mentioned study areas. In the present study, we confirmed the genetic autonomy of the ‘American’ and ‘European’ groups and described the symbionts as Chlorella variabilis Shihira et Krauss and Micractinium reisseri Hoshina, Iwataki et Imamura sp. nov., respectively (Chlorellaceae, Trebouxiophyceae).     

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.     

Population structure of Spodoptera frugiperda maize and rice host forms in South America: are they host strains?

Determining which factors contribute to the formation and maintenance of genetic divergence to evaluate their relative importance as a cause of biological differentiation is among the major challenges in evolutionary biology. In Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) two host strains have been recognized in the 1980s: the corn‐strain prefers maize, sorghum, and cotton, whereas the rice‐strain prefers rice and wild grasses. However, it is not clear to what extent these so‐called ‘strains’, which have also been called ‘host races’ or even ‘sibling species’, are really associated with host plants. Due to the indeterminate evolutionary status, we will use the term ‘host forms’ (sensu Funk). Here, we characterized populations collected from maize, rice, and wild grasses from three countries in South America. Using two mitochondrial cytochrome oxidase I (mtCOI) markers and 10 polymorphisms in the triose phosphate isomerase (Tpi) gene, we found various patterns of host association. Two hundred twenty‐seven nuclear amplified fragment length polymorphisms (AFLPs) markers revealed significant genetic differentiation among populations, which was generally correlated to the host from which the larvae were collected. Using a multivariate discriminant analysis and a Bayesian clustering approach, we found that individuals could be grouped into 2–5 genetically distinct clusters, depending on the method. Together, our results indicate that although host‐associated differentiation is present in this species, it does not account for all observable genetic variation and other factors must be maintaining genetic differentiation between these forms. Therefore, the term ‘host strains’ should be abandoned and ‘host forms’ should be used instead for S. frugiperda.     

Philosophical foundations for the hierarchy of life

We review Evolution and the Levels of Selection by Samir Okasha. This important book provides a cohesive philosophical framework for understanding levels-of-selections problems in biology. Concerning evolutionary transitions, Okasha proposes that three stages characterize the shift from a lower level of selection to a higher one. We discuss the application of Okasha’s three-stage concept to the evolutionary transition from unicellularity to multicellularity in the volvocine green algae. Okasha’s concepts are a provocative step towards a more general understanding of the major evolutionary transitions; however, the application of certain ideas to the volvocine model system is not straightforward.     

On the problem of ecological evolution in <Emphasis Type="Italic">Volvox</Emphasis>

A concept of evolution of ontogeny based on the original data on the comparative biology of Volvox development and published paleoclimatic data is presented. Previously, we have demonstrated that evolutionary reorganizations of asexual development in Volvox are related to the changes in the rate, diel rhythms, and light/dark control of cell divisions. Here, we propose that such rearrangements could take place during much of Cenozoic time (e.g., in Eocene and Miocene) as adaptations to short and warm winter day in high latitudes. This proposal is confirmed by experimental data on culturing Volvox species with different types of development under short photoperiod.     

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.     

microRNAs in a multicellular green alga Volvox carteri

microRNAs(miRNAs)have emerged as key components in the eukaryotic gene regulatory network.We and others have previously identified many miRNAs in a unicellular green alga,Chlamydomonas reinhardtii.To investigate whether miRNA-mediated gene regulation is a general mechanism in green algae and how miRNAs have been evolved in the green algal lineage,we examined small RNAs in Volvox carteri,a multicellular species in the same family with Chlamydomonas reinhardtii.We identified 174 miRNAs in Volvox,with many of them being highly enriched in gonidia or somatic cells.The targets of the miRNAs were predicted and many of them were subjected to miRNA-mediated cleavage in vivo,suggesting that miRNAs play regulatory roles in the biology of green algae.Our catalog of miRNAs and their targets provides a resource for further studies on the evolution,biological functions,and genomic properties of miRNAs in green algae.     

Stable nuclear transformation of Gonium pectorale

Background  

Green algae of the family Volvocaceae are a model lineage for studying the molecular evolution of multicellularity and cellular differentiation. The volvocine alga Gonium is intermediate in organizational complexity between its unicellular relative, Chlamydomonas, and its multicellular relatives with differentiated cell types, such as Volvox. Gonium pectorale consists of ~16 biflagellate cells arranged in a flat plate. The detailed molecular analysis of any species necessitates its accessibility to genetic manipulation, but, in volvocine algae, transformation procedures have so far only been established for Chlamydomonas reinhardtii and Volvox carteri.     

Spatio‐temporal patterns of genome evolution in allotetraploid species of the genus Oryza

Despite knowledge that polyploidy is widespread and a major evolutionary force in flowering plant diversification, detailed comparative molecular studies on polyploidy have been confined to only a few species and families. The genus Oryza is composed of 23 species that are classified into ten distinct ‘genome types’ (six diploid and four polyploid), and is emerging as a powerful new model system to study polyploidy. Here we report the identification, sequence and comprehensive comparative annotation of eight homoeologous genomes from a single orthologous region (Adh1–Adh2) from four allopolyploid species representing each of the known Oryza genome types (BC, CD, HJ and KL). Detailed comparative phylogenomic analyses of these regions within and across species and ploidy levels provided several insights into the spatio‐temporal dynamics of genome organization and evolution of this region in ‘natural’ polyploids of Oryza. The major findings of this study are that: (i) homoeologous genomic regions within the same nucleus experience both independent and parallel evolution, (ii) differential lineage‐specific selection pressures do not occur between polyploids and their diploid progenitors, (iii) there have been no dramatic structural changes relative to the diploid ancestors, (iv) a variation in the molecular evolutionary rate exists between the two genomes in the BC complex species even though the BC and CD polyploid species appear to have arisen <2 million years ago, and (v) there are no clear distinctions in the patterns of genome evolution in the diploid versus polyploid species.     

Genomic insights into the adaptation and evolution of the nautilus,an ancient but evolving “living fossil”

The nautilus, commonly known as a “living fossil,” is endangered and may be at risk of extinction. The lack of genomic information hinders a thorough understanding of its biology and evolution, which can shed light on the conservation of this endangered species. Here, we report the first high-quality chromosome-level genome assembly of Nautilus pompilius. The assembled genome size comprised 785.15 Mb. Comparative genomic analyses indicated that transposable elements (TEs) and large-scale genome reorganizations may have driven lineage-specific evolution in the cephalopods. Remarkably, evolving conserved genes and recent TE insertion activities were identified in N. pompilius, and we speculate that these findings reflect the strong adaptability and long-term survival of the nautilus. We also identified gene families that are potentially responsible for specific adaptation and evolution events. Our study provides unprecedented insights into the specialized biology and evolution of N. pompilius, and the results serve as an important resource for future conservation genomics of the nautilus and closely related species.     

Stable transformation and reverse genetic analysis of Penium margaritaceum: a platform for studies of charophyte green algae,the immediate ancestors of land plants

The charophyte green algae (CGA, Streptophyta, Viridiplantae) occupy a key phylogenetic position as the immediate ancestors of land plants but, paradoxically, are less well‐studied than the other major plant lineages. This is particularly true in the context of functional genomic studies, where the lack of an efficient protocol for their stable genetic transformation has been a major obstacle. Observations of extant CGA species suggest the existence of some of the evolutionary adaptations that had to occur for land colonization; however, to date, there has been no robust experimental platform to address this genetically. We present a protocol for high‐throughput Agrobacterium tumefaciens‐mediated transformation of Penium margaritaceum, a unicellular CGA species. The versatility of Penium as a model for studying various aspects of plant cell biology and development was illustrated through non‐invasive visualization of protein localization and dynamics in living cells. In addition, the utility of RNA interference (RNAi) for reverse genetic studies was demonstrated by targeting genes associated with cell wall modification (pectin methylesterase) and biosynthesis (cellulose synthase). This provided evidence supporting current models of cell wall assembly and inter‐polymer interactions that were based on studies of land plants, but in this case using direct observation in vivo. This new functional genomics platform has broad potential applications, including studies of plant organismal biology and the evolutionary innovations required for transition from aquatic to terrestrial habitats.     

The high‐quality genome of Brassica napus cultivar ‘ZS11’ reveals the introgression history in semi‐winter morphotype

Allotetraploid oilseed rape (Brassica napus L.) is an agriculturally important crop. Cultivation and breeding of B. napus by humans has resulted in numerous genetically diverse morphotypes with optimized agronomic traits and ecophysiological adaptation. To further understand the genetic basis of diversification and adaptation, we report a draft genome of an Asian semi‐winter oilseed rape cultivar ‘ZS11’ and its comprehensive genomic comparison with the genomes of the winter‐type cultivar ‘Darmor‐bzh’ as well as two progenitors. The integrated BAC‐to‐BAC and whole‐genome shotgun sequencing strategies were effective in the assembly of repetitive regions (especially young long terminal repeats) and resulted in a high‐quality genome assembly of B. napus ‘ZS11’. Within a short evolutionary period (~6700 years ago), semi‐winter‐type ‘ZS11’ and the winter‐type ‘Darmor‐bzh’ maintained highly genomic collinearity. Even so, certain genetic differences were also detected in two morphotypes. Relative to ‘Darmor‐bzh’, both two subgenomes of ‘ZS11’ are closely related to its progenitors, and the ‘ZS11’ genome harbored several specific segmental homoeologous exchanges (HEs). Furthermore, the semi‐winter‐type ‘ZS11’ underwent potential genomic introgressions with B. rapa (A_r). Some of these genetic differences were associated with key agronomic traits. A key gene of A03.FLC3 regulating vernalization‐responsive flowering time in ‘ZS11’ was first experienced HE, and then underwent genomic introgression event with A_r, which potentially has led to genetic differences in controlling vernalization in the semi‐winter types. Our observations improved our understanding of the genetic diversity of different B. napus morphotypes and the cultivation history of semi‐winter oilseed rape in Asia.