Long-term Evolutionary Success Research Articles

Evolvability: filling the explanatory gap between adaptedness and the long-term mathematical conception of fitness

The new foundation for the propensity interpretation of fitness (PIF), developed by Pence and Ramsey (Br J Philos Sci 64:851–881, 2013), describes fitness as a probability distribution that encompasses all possible daughter populations to which the organism may give rise, including daughter populations in which traits might change and the possible environments that members of the daughter populations might encounter. This long-term definition of fitness is general enough to avoid counterexamples faced by previous mathematical conceptions of PIF. However, there seem to be downsides to its generality: the ecological role of fitness involves describing the degree of adaptedness between an organism and the specific environment it inhabits. When all possible changes in traits and all possible environments that a daughter population may encounter are included in the concept, it becomes difficult to see how fitness can fulfill this role. In this paper, we argue that this is a feature of Pence and Ramsey’s view rather than a bug: long-term fitness accommodates evolvability considerations, which concern the role that variation plays in evolutionary processes. Building on the foundations, we show that Pence and Ramsey’s fitness—F—can be partitioned into fourths: adaptedness, robustness of adaptedness, and two facets of evolvability. Conceptualizing these last three components forces us to consider the role played by grains of description of both organisms and the environment when thinking about long-term fitness. They track the possibility that there could be a change in type in a daughter population as a way of responding to environmental challenges, or that the type persists in the face of novel environments. We argue that these components are just as salient as adaptedness for long-term fitness. Together, this decomposition of F provides a more accurate picture of the factors involved in long-term evolutionary success.

Chromosome-level genome assembly reveals homologous chromosomes and recombination in asexual rotifer Adineta vaga.

Bdelloid rotifers are notorious as a speciose ancient clade comprising only asexual lineages. Thanks to their ability to repair highly fragmented DNA, most bdelloid species also withstand complete desiccation and ionizing radiation. Producing a well-assembled reference genome is a critical step to developing an understanding of the effects of long-term asexuality and DNA breakage on genome evolution. To this end, we present the first high-quality chromosome-level genome assemblies for the bdelloid Adineta vaga, composed of six pairs of homologous (diploid) chromosomes with a footprint of paleotetraploidy. The observed large-scale losses of heterozygosity are signatures of recombination between homologous chromosomes, either during mitotic DNA double-strand break repair or when resolving programmed DNA breaks during a modified meiosis. Dynamic subtelomeric regions harbor more structural diversity (e.g., chromosome rearrangements, transposable elements, and haplotypic divergence). Our results trigger the reappraisal of potential meiotic processes in bdelloid rotifers and help unravel the factors underlying their long-term asexual evolutionary success.

Evolutionary epidemiology of Streptococcus iniae: Linking mutation rate dynamics with adaptation to novel immunological landscapes

Pathogens continuously adapt to changing host environments where variation in their virulence and antigenicity is critical to their long-term evolutionary success. The emergence of novel variants is accelerated in microbial mutator strains (mutators) deficient in DNA repair genes, most often from mismatch repair and oxidized-guanine repair systems (MMR and OG respectively). Bacterial MMR/OG mutants are abundant in clinical samples and show increased adaptive potential in experimental infection models, yet the role of mutators in the epidemiology and evolution of infectious disease is not well understood. Here we investigated the role of mutation rate dynamics in the evolution of a broad host range pathogen, Streptococcus iniae, using a set of 80 strains isolated globally over 40 years. We have resolved phylogenetic relationships using non-recombinant core genome variants, measured in vivo mutation rates by fluctuation analysis, identified variation in major MMR/OG genes and their regulatory regions, and phenotyped the major traits determining virulence in streptococci. We found that both mutation rate and MMR/OG genotype are remarkably conserved within phylogenetic clades but significantly differ between major phylogenetic lineages. Further, variation in MMR/OG loci correlates with occurrence of atypical virulence-associated phenotypes, infection in atypical hosts (mammals), and atypical (osseous) tissue of a vaccinated primary host. These findings suggest that mutators are likely to facilitate adaptations preceding major diversification events and may promote emergence of variation permitting colonization of a novel host tissue, novel host taxa (host jumps), and immune-escape in the vaccinated host.

Polyspermy in angiosperms: Its contribution to polyploid formation and speciation.

Polyploidization has played a major role in the long-term diversification and evolutionary success of angiosperms. Triploid formation among diploid plants, which is generally considered to be achieved by fertilization of an unreduced gamete with a reduced one, has been accepted as a means of polyploid production. In addition, it has been supposed that polyspermy also contributes to the triploid formation in maize, wheat, and some orchids; however, such a mechanism has been considered uncommon because reproducing the polyspermic situation and unambiguously investigating developmental profiles of polyspermic zygotes are difficult. To overcome these problems, rice polyspermic zygotes have been successfully produced by electrofusion of an egg cell with two sperm cells, and their developmental profiles have been monitored. The triploid zygotes progress through karyogamy and divide into two-celled embryos via a typical bipolar mitotic division; the two-celled embryos further develop into triploid plants, indicating that polyspermic plant zygotes, unlike those of animals, can develop normally. Furthermore, progenies consisting of triparental genetic materials have been successfully obtained in Arabidopsis through the pollination of two different kinds of male parents with a female parent. These different pieces of evidence for development and emergence of polyspermic zygotes in vitro and in planta suggest that polyspermy is a key event in polyploidization and species diversification.

The road to evolutionary success: insights from the demographic history of an Amazonian palm.

Evolutionary success, as demonstrated by high abundance and a wide geographical range, is related to genetic variation and historical demography. Here we assess how climatic change during the Quaternary influenced the demography and distribution of the Neotropical swamp palm Mauritia flexuosa. Using microsatellite loci and coalescent analyses we examined how demographical dynamics affected genetic diversity, effective population size and connectivity through time and space. Mauritia flexuosa presents significant genetic differentiation between the Amazonian and Cerrado biomes and among different river basins. Amazonian lineages are ancient compared to lineages from the Cerrado, a pattern corroborated using the fossil pollen record, where the species was absent from the Cerrado during the cold and dry periods of the last glacial cycles, then returned during the wet, interglacial phases. Coalescent simulations show that the pattern of observed genetic diversity for M. flexuosa is most likely due to a range retraction during the Last Glacial Maximum, leading to multiple refugia and resulting in high differentiation between Amazonian and Cerrado biomes. Isolation-by-distance and by-environment also shaped the distribution and evolutionary success of M. flexuosa. Our study provides new insights into the historical factors that affected geographical distribution and structure genetic diversity, contributing to long-term evolutionary success.

Development of polyspermic zygote and possible contribution of polyspermy to polyploid formation in angiosperms.

Fertilization is a general feature of eukaryotic uni- and multicellular organisms to restore a diploid genome from female and male gamete haploid genomes. In angiosperms, polyploidization is a common phenomenon, and polyploidy would have played a major role in the long-term diversification and evolutionary success of plants. As for the mechanism of formation of autotetraploid plants, the triploid-bridge pathway, crossing between triploid and diploid plants, is considered as a major pathway. For the emergence of triploid plants, fusion of an unreduced gamete with a reduced gamete is generally accepted. In addition, the possibility of polyspermy has been proposed for maize, wheat and some orchids, although it has been regarded as an uncommon mechanism of triploid formation. One of the reasons why polyspermy is regarded as uncommon is because it is difficult to reproduce the polyspermy situation in zygotes and to analyze the developmental profiles of polyspermic triploid zygotes. Recently, polyspermic rice zygotes were successfully produced by electric fusion of an egg cell with two sperm cells, and their developmental profiles were monitored. Two sperm nuclei and an egg nucleus fused into a zygotic nucleus in the polyspermic zygote, and the triploid zygote divided into a two-celled embryo via mitotic division with a typical bipolar microtubule spindle. The two-celled proembryos further developed and regenerated into triploid plants. These suggest that polyspermic plant zygotes have the potential to form triploid embryos, and that polyspermy in angiosperms might be a pathway for the formation of triploid plants.

Formation of triploid plants via possible polyspermy

ABSTRACTPolyploidization is a common phenomenon in angiosperms, and polyploidy has played a major role in the long-term diversification and evolutionary success of plants. Triploid plants are considered as the intermediate stage in the formation of stable autotetraploid plants, and this pathway of tetraploid formation is known as the triploid bridge. As for the mechanism of triploid formation among diploid populations, fusion of an unreduced gamete with a reduced gamete is generally accepted. In addition, the possibility of polyspermy has been proposed for maize, wheat and some orchids, although it has been regarded as an uncommon mechanism of polyploid formation. One of the reasons why polyspermy is regarded as uncommon is because it is difficult to reproduce the polyspermy situation in zygotes and to analyze the developmental profiles of polyspermic zygotes. In the study, we produced polyspermic rice zygotes by electric fusion of an egg cell with two sperm cells and monitored their developmental profiles. The two sperm nuclei and the egg nucleus fused into a zygotic nucleus in the polyspermic zygote, and the triploid zygote divided into a two-celled embryo via mitotic division with a typical bipolar microtubule spindle. The two-celled proembryos developed and regenerated into triploid plants. These results suggest that polyspermic plant zygotes have the potential to form triploid embryos, and that polyspermy in angiosperms might be a pathway for the formation of triploid plants.

Totemism and long-term evolutionary success.

Totemism and long-term evolutionary success.

Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota).

Microbial symbionts are instrumental to the ecological and long-term evolutionary success of their hosts, and the central role of symbiotic interactions is increasingly recognized across the vast majority of life. Lichens provide an iconic group for investigating patterns in species interactions; however, relationships among lichen symbionts are often masked by uncertain species boundaries or an inability to reliably identify symbionts. The species-rich lichen-forming fungal family Parmeliaceae provides a diverse group for assessing patterns of interactions of algal symbionts, and our study addresses patterns of lichen symbiont interactions at the largest geographic and taxonomic scales attempted to date. We analysed a total of 2356 algal internal transcribed spacer (ITS) region sequences collected from lichens representing ten mycobiont genera in Parmeliaceae, two genera in Lecanoraceae and 26 cultured Trebouxia strains. Algal ITS sequences were grouped into operational taxonomic units (OTUs); we attempted to validate the evolutionary independence of a subset of the inferred OTUs using chloroplast and mitochondrial loci. We explored the patterns of symbiont interactions in these lichens based on ecogeographic distributions and mycobiont taxonomy. We found high levels of undescribed diversity in Trebouxia, broad distributions across distinct ecoregions for many photobiont OTUs and varying levels of mycobiont selectivity and specificity towards the photobiont. Based on these results, we conclude that fungal specificity and selectivity for algal partners play a major role in determining lichen partnerships, potentially superseding ecology, at least at the ecogeographic scale investigated here. To facilitate effective communication and consistency across future studies, we propose a provisional naming system for Trebouxia photobionts and provide representative sequences for each OTU circumscribed in this study.

Allele Sharing and Evidence for Sexuality in a Mitochondrial Clade of Bdelloid Rotifers.

Rotifers of Class Bdelloidea are common freshwater invertebrates of ancient origin whose apparent asexuality has posed a challenge to the view that sexual reproduction is essential for long-term evolutionary success in eukaryotes and to hypotheses for the advantage of sex. The possibility nevertheless exists that bdelloids reproduce sexually under unknown or inadequately investigated conditions. Although certain methods of population genetics offer definitive means for detecting infrequent or atypical sex, they have not previously been applied to bdelloid rotifers. We conducted such a test with bdelloids belonging to a mitochondrial clade of Macrotrachela quadricornifera. This revealed a striking pattern of allele sharing consistent with sexual reproduction and with meiosis of an atypical sort, in which segregation occurs without requiring homologous chromosome pairs.

The horseshoe crab of the genus Limulus: living fossil or stabilomorph?

A new horseshoe crab species, Limulus darwini, is described from the uppermost Jurassic (ca. 148 Ma) near-shore sediments of the Kcynia Formation, central Poland. The only extant species Limulus polyphemus (Linnaeus) inhabits brackish-marine, shallow water environments of the east coast of the United States. Here it is shown that there are no important morphological differences between the Kcynia Formation specimens and extant juvenile representatives of the genus Limulus. The palaeoecological setting inhabited by the new species and the trophic relationships of extant horseshoe crabs are discussed in an attempt to determine the potential range of food items ingested by these Mesozoic xiphosurans. In this paper we propose the adoption of a new term stabilomorphism, this being: an effect of a specific formula of adaptative strategy among organisms whose taxonomic status does not exceed genus-level. A high effectiveness of adaptation significantly reduces the need for differentiated phenotypic variants in response to environmental changes and provides for long-term evolutionary success.

Multiple hybridization events in Cardamine (Brassicaceae) during the last 150 years: revisiting a textbook example of neoallopolyploidy

Recently formed allopolyploid species represent excellent subjects for exploring early stages of polyploid evolution. The hexaploid Cardamine schulzii was regarded as one of the few nascent allopolyploid species formed within the past ∼150 years that presumably arose by autopolyploidization of a triploid hybrid, C. × insueta; however, the most recent investigations have shown that it is a trigenomic hybrid. The aims of this study were to explore the efficiency of progenitor-specific microsatellite markers in detecting the hybrid origins and genome composition of these two allopolyploids, to estimate the frequency of polyploid formation events, and to outline their evolutionary potential for long-term persistence and speciation. Flow-cytometric ploidy-level screening and genotyping by progenitor-specific microsatellite markers (20 microsatellite loci) were carried out on samples focused on hybridizing populations at Urnerboden, Switzerland, but also including comparative material of the parental species from other sites in the Alps and more distant areas. It was confirmed that hybridization between the diploids C. amara and C. rivularis auct. gave rise to triploid C. × insueta, and it is inferred that this has occurred repeatedly. Evidence is provided that C. schulzii comprises three parental genomes and supports its origin from hybridization events between C. × insueta and the locally co-occurring hypotetraploid C. pratensis, leading to two cytotypes of C. schulzii: hypopentaploid and hypohexaploid. Each cytotype of C. schulzii is genetically uniform, suggesting their single origins. Persistence of C. schulzii has presumably been achieved only by perennial growth and clonal reproduction. This contrasts with C. × insueta, in which multiple origins and occasional sexual reproduction have generated sufficient genetic variation for long-term survival and evolutionary success. This study illustrates a complex case of recurrent hybridization and polyploidization events, and highlights the role of triploids that promoted the origin of trigenomic hybrids.

Long-term evolution is surprisingly predictable in lattice proteins

It has long been debated whether natural selection acts primarily upon individual organisms, or whether it also commonly acts upon higher-level entities such as lineages. Two arguments against the effectiveness of long-term selection on lineages have been (i) that long-term evolutionary outcomes will not be sufficiently predictable to support a meaningful long-term fitness and (ii) that short-term selection on organisms will almost always overpower long-term selection. Here, we use a computational model of protein folding and binding called 'lattice proteins'. We quantify the long-term evolutionary success of lineages with two metrics called the k-fitness and k-survivability. We show that long-term outcomes are surprisingly predictable in this model: only a small fraction of the possible outcomes are ever realized in multiple replicates. Furthermore, the long-term fitness of a lineage depends only partly on its short-term fitness; other factors are also important, including the 'evolvability' of a lineage-its capacity to produce adaptive variation. In a system with a distinct short-term and long-term fitness, evolution need not be 'short-sighted': lineages may be selected for their long-term properties, sometimes in opposition to short-term selection. Similar evolutionary basins of attraction have been observed in vivo, suggesting that natural biological lineages will also have a predictive long-term fitness.

Genetic evaluation of the initiation of a captive population: the general approach and a case study in the endangered pallid sturgeon (Scaphirhynchus albus)

Because of recent environmental changes, a number of species have become critically endangered in the wild. To prevent extinction of these species, captive populations have been established and generally maintained in a manner that attempts to avoid detrimental genetic changes. In particular, wild founders should be unrelated and not inbred. The subsequent generations in captivity should make the effective population size as large as possible to retain the initial genetic variation. Pallid sturgeon (Scaphirhynchus albus) from the upper Missouri River USA have not successfully recruited in decades. Perpetuation of this stock is now accomplished through captive spawning of wild-caught fish with subsequent release of their offspring. In addition to the fish released into the wild, more than 2,000 offspring of the wild fish from 11 year-classes are captively housed. We examined the genetic risks associated with using these fish as a captive population for the future propagation of pallid sturgeon and concluded that the wild individuals are unrelated, non-inbred remnants of a formerly larger population. Further, there is a sufficiently large effective population size (Ne) present in the captive broodstock for propagation provided that the effective population size can be increased in subsequent generations. This study shows how genetic and evolutionary principles and applications can be used to evaluate the potential founders of a captive population and make recommendations for the long-term evolutionary success of an endangered species.

Angiosperm polyploids and their road to evolutionary success

The abundance of polyploidy among flowering plants has long been recognized, and recent studies have uncovered multiple ancient polyploidization events in the evolutionary history of several angiosperm lineages. Once polyploids are formed they must get locally established and then propagate and survive while adapting to different environments and avoiding extinction. This might ultimately lead to their long-term evolutionary success, where their descendant lineages survive for tens of millions of years. Along this road to evolutionary success, polyploids must overcome several obstacles, to which several genetic and ecological factors are likely to contribute. One recurrent observation, based on present-day polyploids, has been the high frequency of polyploids in harsh environments. Also, recent studies proposed that the success of certain ancient polyploids might be linked to periods of climatic change. Although we are still in the early stages of unraveling the factors that resulted in the long-term evolutionary success of ancient polyploids, the advances in genomic sequencing and molecular dating methods promise to enhance our understanding. It, therefore, seems timely to review our current knowledge of what determines the success of polyploids. Here, we discuss especially how harsh conditions or periods of climatic change might affect the rate of formation, establishment, persistence and long-term evolutionary success of polyploids in angiosperms.

Rapid genomic changes in polyploid wheat and related species: implications for genome evolution and genetic improvement

A polyploid organism by possessing more than two sets of chromosomes from one species (autopolyploidy) or two or more species (allopolyploidy) is known to have evolutionary advantages. However, by what means a polyploid accommodates increased genetic dosage or divergent genomes (allopolyploidy) in one cell nucleus and cytoplasm constitutes an enormous challenge. Recent years have witnessed efforts and progress in exploring the possible mechanisms by which these seemingly intangible hurdles of polyploidy may be ameliorated or eventually overcome. In particular, the documentation of rapid and extensive non-Mendelian genetic and epigenetic changes that often accompany nascent polyploidy is revealing: the resulting non-additive and novel gene expression at global, regional and local levels, and timely restoration of meiotic chromosomal behavior towards bivalent pairing and disomic inheritance may ensure rapid establishment and stabilization as well as its long-term evolutionary success. Further elucidation on these novel mechanisms underpinning polyploidy will promote our understanding on fundamental issues in evolutionary biology and in our manipulation capacities in future genetic improvement of important crops that are currently polyploids in genomic constitution. This review is intended to provide an updated discussion on these interesting and important issues within the scope of a specific yet one of the most important plant groups-polyploid wheat and its related species.

Evolutionary coupling between the deleteriousness of gene mutations and the amount of non-coding sequences

The phenotypic effects of random mutations depend on both the architecture of the genome and the gene–trait relationships. Both levels thus play a key role in the mutational variability of the phenotype, and hence in the long-term evolutionary success of the lineage. Here, by simulating the evolution of organisms with flexible genomes, we show that the need for an appropriate phenotypic variability induces a relationship between the deleteriousness of gene mutations and the quantity of non-coding sequences maintained in the genome. The more deleterious the gene mutations, the shorter the intergenic sequences. Indeed, in a shorter genome, fewer genes are affected by rearrangements (duplications, deletions, inversions, translocations) at each replication, which compensates for the higher impact of each gene mutation. This spontaneous adjustment of genome structure allows the organisms to retain the same average fitness loss per replication, despite the higher impact of single gene mutations. These results show how evolution can generate unexpected couplings between distinct organization levels.

Cryptic sex and many-to-one coevolution in the fungus-growing ant symbiosis.

The fungus-growing ants have long provided a spectacular example of coevolutionary integration. Their ecological success is thought to depend largely on the evolutionary alignment of reproductive interests between ants and fungi after vertical transmission and the ancient suppression of fungal sexuality. In the present study we test these assumptions and provide the first evidence of recombination in attine cultivars, contradicting widely held perceptions of obligate clonality. In addition, we document long-distance horizontal transmission of symbionts between leaf-cutter ant species on mainland Central America and South America and those endemic to Cuba, suggesting both lack of pairwise coevolutionary specificity in ant/cultivar interactions and dispersal of symbionts independent of their ant hosts. The coevolution between leaf-cutters and their fungal symbionts is thus not reciprocally pairwise. Rather, a single widespread and sexual fungal symbiont species is engaged in multiple interactions with divergent ant lineages. Strict fungal clonality and vertical transmission evidently have not played a critical role in the long-term evolutionary or ecological success of this well known mutualism.

Ecological and evolutionary opportunities of apomixis: insights from Taraxacum and Chondrilla.

The ecological and evolutionary opportunities of apomixis in the short and the long term are considered, based on two closely related apomictic genera: Taraxacum (dandelion) and Chondrilla (skeleton weed). In both genera apomicts have a wider geographical distribution than sexuals, illustrating the short-term ecological success of apomixis. Allozymes and DNA markers indicate that apomictic populations are highly polyclonal. In Taraxacum, clonal diversity can be generated by rare hybridization between sexuals and apomicts, the latter acting as pollen donors. Less extensive clonal diversity is generated by mutations within clonal lineages. Clonal diversity may be maintained by frequency-dependent selection, caused by biological interactions (e.g. competitors and pathogens). Some clones are geographically widespread and probably represent phenotypically plastic 'general-purpose genotypes'. The long-term evolutionary success of apomictic clones may be limited by lack of adaptive potential and the accumulation of deleterious mutations. Although apomictic clones may be considered as 'evolutionary dead ends', the genes controlling apomixis can escape from degeneration and extinction via pollen in crosses between sexuals and apomicts. In this way, apomixis genes are transferred to a new genetic background, potentially adaptive and cleansed from linked deleterious mutations. Consequently, apomixis genes can be much older than the clones they are currently contained in. The close phylogenetic relationship between Taraxacum and Chondrilla and the similarity of their apomixis mechanisms suggest that apomixis in these two genera could be of common ancestry.

Adaptive Radiation in Insects and Plants: Time and Opportunity

SYNOPSIS. Insects and their hostplants represent the major part of terrestrial diversity, yet we are just beginning to understand why there are so very many species. By far the most influential model of insect/plant diversification has been Ehrlich and Raven's (1964) hypothesis of insect/plant coevolution. While the coevolution model was based on macroevolutionary patterns in plant defenses and hostplant affiliations, most of the subsequent work has been on its possible ecological and genetic mechanisms, with relatively little systematic scrutiny of the evolutionary patterns Ehrlich and Raven described. We explore the possible roles insect/plant interactions may play in the long-term evolution of insect and plant lineages, and review some of the evidence on whether or not insects and plants have exerted reciprocal influences on each other's diversification. Insects and plants have diversified over roughly the same time intervals, and many insect host/affiliations are evolutionarily conserved, thus reflecting long/term, phylogenetic history. Rather than accumulating herbivores at a rate proportional to their geographic area of distribution or biomass, some plant groups pose apparent chemical barriers to potential herbivore colonists, and seem accessible to relatively few insect lineages, possibly preadapted by use of chemically similar or related hostplants. Evolutionary innovations in plant defenses and in insect feeding habits seem to have spurred their respective adaptive radiations, thus ecological opportunity may influence long-term evolutionary success. The greater diversity of insects and plants in the tropics, compared to the temperate zone, probably reflects the greater age of tropical habitats as well as climatic barriers that limit successful invasion of the temperate zone to just those primitively tropical groups able to evolve strategies for both overwintering and use of temperate resources. Though evidence is still sparse, successful invasion of the temperate zone may promote subsequent radiations of both insects and plants. We conclude that much of the available evidence from systematics is consistent with Ehrlich and Raven's suggestion that much of insect and plant diversification has been spurred by a series of ecological opportunities over evolutionary time.