LIVE-BIRTH IN VIPERS (VIPERIDAE) IS A KEY INNOVATION AND ADAPTATION TO GLOBAL COOLING DURING THE CENOZOIC

The identification of adaptations and key innovations has long interested biologists because they confer on organisms the ability to exploit previously unavailable ecological resources and respond to novel selective pressures. Although it can be extremely difficult to test for the effects of a character on the rate of lineage diversification, the convergent evolution of a character in multiple lineages provides an excellent opportunity to test for the effect of that character on lineage diversification. Here, I examine the effect of parity mode on the diversification of vipers, which have independently evolved viviparity in at least 13 lineages. I find strong statistical evidence that viviparous species diversify at a greater rate than oviparous species and correlate major decreases in the diversification rate of oviparous species with periods of global cooling, such as the Oligocene. These results suggest that the evolution of viviparity buffered live-bearing species against the negative effects of global climate change during the Cenozoic, and was a key innovation in the evolution and diversification of live-bearing vipers.     

How plants conquered land: evolution of terrestrial adaptation

The transition of plants from water to land is considered one of the most significant events in the evolution of life on Earth. The colonization of land by plants, accompanied by their morphological, physiological and developmental changes, resulted in plant biodiversity. Besides significantly influencing oxygen levels in the air and on land, plants manufacture organic matter from CO₂ and water with the help of sunlight, paving the way for the diversification of nonplant lineages ranging from microscopic organisms to animals. Land plants regulate the climate by adjusting total biomass and energy flow. At the genetic level, these innovations are achieved through the rearrangement of pre-existing genetic information. Advances in genome sequencing technology are revamping our understanding of plant evolution. This study highlights the morphological and genomic innovations that allow plants to integrate life on Earth.     

Effects of gasteroid fruiting body morphology on diversification rates in three independent clades of fungi estimated using binary state speciation and extinction analysis

Gasteroid fungi include puffballs, stinkhorns, and other forms that produce their spores inside the fruiting body. Gasteroid taxa comprise about 8.4% of the Agaricomycetes (mushroom-forming fungi) and have evolved numerous times from nongasteroid ancestors, such as gilled mushrooms, polypores, and coral fungi, which produce spores on the surface of the fruiting body. Nongasteroid Agaricomycetes have a complex mechanism of forcible spore discharge that is lost in gasteroid lineages, making reversals to nongasteroid forms very unlikely. Our objective was to determine whether gasteromycetation affects the rate of diversification of lineages "trapped" in the gasteroid state. We assembled four datasets (the Sclerodermatineae, Boletales, Phallomycetidae, and Lycoperdaceae), representing unique origins of gasteroid fungi from nongasteroid ancestors and generated phylogenies using BEAST. Using the program Diversitree, we analyzed these phylogenies to estimate character-state-specific rates of speciation and extinction, and rates of transitions between nongasteroid and gasteroid forms. Most optimal models suggest that the net diversification rate of gasteroid forms exceeds that of nongasteroid forms, and that gasteroid forms will eventually come to predominate over nongasteroid forms in the clades in which they have arisen. The low frequency of gasteroid forms in the Agaricomycetes as a whole may reflect the recent origins of many gasteroid lineages.     

The origin of metazoan development: a palaeobiological perspective

The rapid diversification of early Metazoa remains one of the most puzzling events in the fossil record. Several models have been proposed to explain a critical aspect of this event: the origin of Metazoan development. These include the origin of the eukaryotic cell, environmental triggers, key innovations or selection among cell lineages. Here, the first three hypotheses are evaulated within a phylogenetic framework using fossil, molecular and developmental evidence. Many elements of metazoan development are widely distributed among unicellular eukaryotes, yet only 3 of the 23 multicellular eukaryotic lineages evolved complex development. Molecular evidence indicates the lineage leading to the eukaryotic cell is nearly as old as the eubacterial and archaebacterial lineages, although the symbiotic events established that the eukaryotic cell probably occurred about 1.5 billion years ago. Yet Metazoa did not appear until 1000 to 600 million years ago (Myr), suggesting the origin of metazoan development must be linked to either an environmental trigger, perhaps an increase in atmospheric oxygen, or key innovations such as the development of collagen. Yet the first model fails to explain the unique appearance of complex development in Metazoa, while the latter fails to explain the simultaneous diversification of several ‘protist’ groups along with the Metazoa. A more complete model of the origin of metazoan development combines environmental triggering of a series of innovations, with successive innovations generating radiations of metazoan clades as lineages breached functional thresholds. The elaboration of new cell classes and the appearance of such developmental innovations as cell sheets may have been of particular importance. Evolutionary biologists often implicitly assume that evolution is a uniformitarian, time-homogeneous process without strong temporal asymmetries in evolutionary mechanisms, rate or context. Yet evolutionary patterns do exhibit such asymmetries, raising the possibility that such innovations as metazoan development impose non-uniformities of evolutionary process.     

Influences of environmental factors on fruiting body induction,development and maturation in mushroom-forming fungi

Mushroom-forming fungi (restricted to basidiomycetous fungi in this review) differentiate by sensing several environmental factors for fruiting body formation. For fruiting body induction, nutrient, temperature and light conditions are critical environmental factors. Higher nitrogen and carbon sources in the media will suppress fruiting body induction in many mushroom-forming fungi, with induction being triggered by lower nitrogen and carbon concentrations. Low temperature or temperature downshift is another critical influencing factor for fruiting body induction in many cultivated mushrooms, such as Flammulina velutipes, Lentinula edodes, and Volvariella volvacea. Fungal response toward starvation and cold involves the production of sexual spores as the next generation. Species like F. velutipes and Coprinopsis cinerea can form fruiting bodies in the dark; however, light accelerates fruiting body induction in some mushroom-forming fungi. Remarkably, fruiting bodies formed in the dark have tiny or no pileus on heads (called dark stipe, pinhead fruiting body, or etiolated stipe). Light is essential for pileus differentiation in many, but not all mushroom species; one exception is Agaricus bisporus. Mushrooms have positive phototropism and negative gravitropism for effective dispersal of spores. Carbon dioxide concentrations also affect fruiting body development; pileus differentiation is suppressed at a high concentration of carbon dioxide. Thus, the pileus differentiation system of mushrooms may allow the most effective diffusion of spores. Full expansion of the pileus is followed by pileus autolysis or senescence. In C. cinerea, pileus autolysis occurs during spore diffusion. Fruiting body senescence, browning of gill, and softening occur after harvesting in several mushroom species. Fruiting body induction, development, and maturation in mushroom-forming fungi are discussed in this review.     

MORPHOLOGICAL RATES OF ANGIOSPERM SEED SIZE EVOLUTION

The evolution of seed size among angiosperms reflects their ecological diversification in a complex fitness landscape of life‐history strategies. The lineages that have evolved seeds beyond the upper and lower boundaries that defined nonflowering seed plants since the Paleozoic are more dispersed across the angiosperm phylogeny than would be expected under a neutral model of phenotypic evolution. Morphological rates of seed size evolution estimated for 40 clades based on 17,375 species ranged from 0.001 (Garryales) to 0.207 (Malvales). Comparative phylogenetic analysis indicated that morphological rates are not associated with the clade's seed size but are negatively correlated with the clade's position in the overall distribution of angiosperm seed sizes; clades with seed sizes closer to the angiosperm mean had significantly higher morphological rates than clades with extremely small or extremely large seeds. Likewise, per‐clade taxonomic diversification rates are not associated with the seed size of the clade but with where the clade falls within the angiosperm seed size distribution. These results suggest that evolutionary rates (morphological and taxonomic) are elevated in densely occupied regions of the seed morphospace relative to lineages whose ecophenotypic innovations have moved them toward the edges.     

Courting disaster: How diversification rate affects fitness under risk

Life is full of risk. To deal with this uncertainty, many organisms have evolved bet-hedging strategies that spread risk through phenotypic diversification. These rates of diversification can vary by orders of magnitude in different species. Here we examine how key characteristics of risk and organismal ecology affect the fitness consequences of variation in diversification rate. We find that rapid diversification is strongly favored when the risk faced has a wide spatial extent, with a single disaster affecting a large fraction of the population. This advantage is especially great in small populations subject to frequent disaster. In contrast, when risk is correlated through time, slow diversification is favored because it allows adaptive tracking of disasters that tend to occur in series. Naturally evolved diversification mechanisms in diverse organisms facing a broad array of environmental risks largely support these results. The theory presented in this article provides a testable ecological hypothesis to explain the prevalence of slow stochastic switching among microbes and rapid, within-clutch diversification strategies among plants and animals.     

Divergence pattern of animal gene families and relationship with the Cambrian explosion

There are many gene families that are specific to multicellular animals. These have either diverged from ancestral genes that are shared with fungi and/or plants or evolved from an ancestral gene unique to animals. The evolution of gene families involved in cell–cell communication and developmental control has been studied to establish whether the number of member genes increased dramatically immediately prior to or in concert with the Cambrian explosion. A molecular phylogeny‐based analysis of several animal‐specific gene families has revealed that gene diversification by duplication occurred during two active periods interrupted by a long intervening quiescent period. Intriguingly, the Cambrian explosion is situated in the silent period, indicating that there is no direct link between the first burst of gene diversification and the Cambrian explosion itself. The importance of gene recruitment as a possible molecular mechanism for morphological diversity, and its possible role for the Cambrian explosion, are discussed. BioEssays 23:1018–1027, 2001. © 2001 John Wiley & Sons, Inc.     

Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes

Sequence similarity and profile searching tools were used to analyze the genome sequences of Arabidopsis thaliana, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Caenorhabditis elegans and Drosophila melanogaster for genes encoding three families of histone deacetylase (HDAC) proteins and three families of histone acetyltransferase (HAT) proteins. Plants, animals and fungi were found to have a single member of each of three subfamilies of the GNAT family of HATs, suggesting conservation of these functions. However, major differences were found with respect to sizes of gene families and multi-domain protein structures within other families of HATs and HDACs, indicating substantial evolutionary diversification. Phylogenetic analysis identified a new class of HDACs within the RPD3/HDA1 family that is represented only in plants and animals. A similar analysis of the plant-specific HD2 family of HDACs suggests a duplication event early in dicot evolution, followed by further diversification in the lineage leading to Arabidopsis. Of three major classes of SIR2-type HDACs that are found in animals, fungi have representatives only in one class, whereas plants have representatives only in the other two. Plants possess five CREB-binding protein (CBP)-type HATs compared with one to two in animals and none in fungi. Domain and phylogenetic analyses of the CBP family proteins showed that this family has evolved three distinct types of CBPs in plants. The domain architecture of CBP and TAF(II)250 families of HATs show significant differences between plants and animals, most notably with respect to bromodomain occurrence and their number. Bromodomain-containing proteins in Arabidopsis differ strikingly from animal bromodomain proteins with respect to the numbers of bromodomains and the other types of domains that are present. The substantial diversification of HATs and HDACs that has occurred since the divergence of plants, animals and fungi suggests a surprising degree of evolutionary plasticity and functional diversification in these core chromatin components.     

The evolution of plant development

The last decade has witnessed a resurgence in the study of the evolution of plant development, combining investigations in systematics, developmental morphology, molecular developmental genetics, and molecular evolution. The integration of phylogenetic studies, structural analyses of fossil and extant taxa, and molecular developmental genetic information allows the formulation of explicit and testable hypotheses for the evolution of morphological characters. These comprehensive approaches provide opportunities to dissect the evolution of major developmental transitions among land plants, including those associated with apical meristems, the origins of the root/shoot dichotomy, diversification of leaves, and origin and subsequent modification of flower structure. The evolution of these major developmental innovations is discussed within both phylogenetic and molecular genetic contexts. We conclude that it is the combination of these approaches that will lead to the greatest understanding of the evolution of plant development.     

Induction of β-1,3-glucanase in seeds of maize defective-kernel mutant (827Kpro1)

β-1,3-glucanases are found in organisms as diverse as plants, animals, bacteria and fungi. In plants, such enzymes are not only associated with defense mechanisms against pathogens, but also play critical roles in physiological and developmental processes. Here we identified a new β-1,3-glucanase in maize seeds, and named it ZmGlucA. Sequence analysis revealed that ZmGlucA belongs to the class A of β-1,3-glucanase, a class related to defense and physiological processes in plants. mRNA and protein assays showed that zmGlucA is expressed exclusively in seeds, and it is differentially regulated during seed development. Additionally, zmGlucA expression is strongly induced in seeds of the mutant dek 827Kpro1, which is defective for embryo and endosperm development. Our data support the idea that ZmGlucA protein is relevant to seed development.     

Male pregnancy in seahorses and pipefish: beyond the mammalian model

Pregnancy has been traditionally defined as the period during which developing embryos are incubated in the body after egg-sperm union. Despite strong similarities between viviparity in mammals and other vertebrate groups, researchers have historically been reluctant to use the term pregnancy for non-mammals in recognition of the highly developed form of viviparity in eutherians. Syngnathid fishes (seahorses and pipefishes) have a unique reproductive system, where the male incubates developing embryos in a specialized brooding structure in which they are aerated, osmoregulated, protected and likely provisioned during their development. Recent insights into physiological, morphological and genetic changes associated with syngnathid reproduction provide compelling evidence that male incubation in these species is a highly specialized form of reproduction akin to other forms of viviparity. Here, we review these recent advances, highlighting similarities and differences between seahorse and mammalian pregnancy. Understanding the changes associated with the parallel evolution of male pregnancy in the two major syngnathid lineages will help to identify key innovations that facilitated the development of this unique form of reproduction and, through comparison with other forms of live bearing, may allow the identification of a common set of characteristics shared by all viviparous organisms.     

Viviparity Advantages in the Lizard <Emphasis Type="Italic">Liolaemus sarmientoi</Emphasis> from the End of the World

Two hypotheses have prevailed to explain the evolution of viviparity in reptiles: the first proposed that viviparity evolved in response to cold-climates because the possibility of pregnant females to thermoregulate at higher temperatures than embryos could experience in a nest in nature. The second hypothesis posits that the advantage of viviparity is based on the possibility of females to maintain stable body temperatures during development, enhancing offspring fitness. With the aim to contribute to understanding the origins of viviparity in reptiles, we experimentally subjected pregnant females of the austral lizard Liolaemus sarmientoi to two temperature treatments until parturition: one that simulated environmental temperatures for a potential nest (17–25?°C) and another that allowed females to thermoregulate at their preferred body temperature (17–45?°C). Then, we analysed newborn body conditions and their locomotor performance to estimate their fitness. In addition, we measured the body temperature in the field and the preferred temperature in the laboratory of pregnant and non-pregnant females. Pregnant females thermoregulated to achieve higher temperatures than the environmental temperatures, and also thermoregulated within a narrower range than non-pregnant females. This could have allowed embryos to develop in higher and more stable temperatures than they would experience in a nest in nature. Thus, offspring developed at the female preferred temperature showed greater fitness and were born earlier in the season than those developed at lower environmental temperatures. Herein, we show that results are in agreement with the two hypotheses of the origin of viviparity for one of the southernmost lizards of the world.     

Thermoregulation during gravidity in the children's python (Antaresia childreni): a test of the preadaptation hypothesis for maternal thermophily in snakes

Pregnant squamate reptiles (i.e. lizards and snakes) often maintain higher and more stable body temperatures than their nonpregnant conspecifics, and this maternal thermophily enhances developmental rate and can lead to increased offspring quality. However, it is unclear when this behaviour evolved relative to the evolution of viviparity. A preadaptation hypothesis suggests that maternal thermophily was a preadaptation to viviparity. Oviparous squamates are unique among oviparous reptiles for generally retaining their eggs until the embryos achieve one fourth of their development. As a result, maternal thermophily by gravid squamates may provide the same thermoregulatory benefits, at least during early development, that have been associated with viviparity. Thus, the evolution of viviparity in squamates may reflect an expanded duration of a pre-existing maternal thermoregulatory behaviour. Despite its evolutionary relevance, thermoregulation during gravidity in oviparous squamates has not yet been explored in depth. In the present study, we examined whether gravidity was associated with thermoregulatory changes in the oviparous children's python, Antaresia childreni . First, we discovered that, compared to most snakes, A. childreni is at an advanced stage of embryonic development at oviposition. Second, using surgically implanted temperature loggers, we detected a significant influence of reproductive status on thermoregulation. Reproductive females maintained higher and less variable body temperatures than nonreproductive females and this difference was most pronounced during the last 3 weeks of gravidity. Overall, these results highlight the continuum between oviparity and viviparity in squamate reptiles and emphasize the importance of thermal control of early embryonic development independent of reproductive mode.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 499–508.     

Complex multicellularity in fungi: evolutionary convergence,single origin,or both?

Complex multicellularity represents the most advanced level of biological organization and it has evolved only a few times: in metazoans, green plants, brown and red algae and fungi. Compared to other lineages, the evolution of multicellularity in fungi follows different principles; both simple and complex multicellularity evolved via unique mechanisms not found in other lineages. Herein we review ecological, palaeontological, developmental and genomic aspects of complex multicellularity in fungi and discuss general principles of the evolution of complex multicellularity in light of its fungal manifestations. Fungi represent the only lineage in which complex multicellularity shows signatures of convergent evolution: it appears 8–11 times in distinct fungal lineages, which show a patchy phylogenetic distribution yet share some of the genetic mechanisms underlying complex multicellular development. To explain the patchy distribution of complex multicellularity across the fungal phylogeny we identify four key observations: the large number of apparently independent complex multicellular clades; the lack of documented phenotypic homology between these clades; the conservation of gene circuits regulating the onset of complex multicellular development; and the existence of clades in which the evolution of complex multicellularity is coupled with limited gene family diversification. We discuss how these patterns and known genetic aspects of fungal development can be reconciled with the genetic theory of convergent evolution to explain the pervasive occurrence of complex multicellularity across the fungal tree of life.     

Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria

Multicellular forms of life have evolved many times, independently giving rise to a diversity of organisms such as animals, plants, and fungi that together comprise the visible biosphere. Yet multicellular life is far more widespread among eukaryotes than just these three lineages. A particularly common form of multicellularity is a social aggregative fruiting lifestyle whereby individual cells associate to form a "fungus-like" sorocarp. This complex developmental process that requires the interaction of thousands of cells working in concert was made famous by the "cellular slime mold"Dictyostelium discoideum, which became an important model organism. Although sorocarpic protistan lineages have been identified in five of the major eukaryote groups, the ubiquitous and globally distributed species Guttulinopsis vulgaris has eluded proper classification. Here we demonstrate, by phylogenomic analyses of a 159-protein data set, that G. vulgaris is a member of Rhizaria and is thus the first member of this eukaryote supergroup known to be capable of aggregative multicellularity.     

HETEROCHRONY AND DEVELOPMENTAL INNOVATION: EVOLUTION OF FEMALE GAMETOPHYTE ONTOGENY IN GNETUM,A HIGHLY APOMORPHIC SEED PLANT

Seed plant female gametophytes are focal points for the evolutionary modification of development. From a structural perspective, the most divergent female gametophytes among all seed plants are found in Gnetum, a clade within Gnetales. Coenocytic organization at sexual maturity, absence of defined egg cells (free nuclei are fertilized), lack of centripetal cellularization, and postfertilization development of embryo-nourishing tissues are features of the female gametophytes of Gnetum unparalleled among seed plants. Although the female gametophyte of Gnetum retains the three basic phases of somatic development common to female gametophytes of plesiomorphic seed plants (free nuclear development, cellularization, cellular growth), the timing of fertilization has been accelerated relative to the rate of somatic development. As a consequence, the female gametophyte of Gnetum matures sexually (is fertilized) at a juvenile (compared with the ancestral somatic ontogeny) and free nuclear stage of somatic development, thereby precluding differentiation of egg cells. Unlike progenetic animals, where truncation of somatic ontogeny evolves in tandem with acceleration in the timing of sexual maturation, the female gametophyte of Gnetum completes the entire ancestral somatic ontogeny after precocious sexual maturation. This results in the evolution of postfertilization development of embryo-nourishing female gametophyte tissues, a phenomenon unique among seed plants. Nonheterochronic developmental innovations have also played important roles in the evolution of the female gametophyte of Gnetum. Centripetal cellularization, which is always associated with the phase change from coenocytic to cellular organization among plesiomorphic seed plant female gametophytes, is lacking in Gnetum. Instead, during early phases of development, apomorphic free nuclear organization is coupled with a highly anomalous pattern of cellularization. Stage-specific innovations during early development in the female gametophyte of Gnetum do not affect plesiomorphic aspects of later phases of development. Thus, a complex array of heterochronic and nonheterochronic developmental innovations have played critical roles in the ontogenetic evolution of the highly apomorphic female gametophyte of Gnetum.