The development of an Arabidopsis model system for genome-wide analysis of polyploidy effects

Arabidopsis is a model system not only for studying numerous aspects of plant biology, but also for understanding mechanisms of the rapid evolutionary process associated with genome duplication and polyploidization. Although in animals interspecific hybrids are often sterile and aneuploids are related to disease syndromes, both Arabidopsis autopolyploids and allopolyploids occur in nature and can be readily formed in the laboratory, providing an attractive system for comparing changes in gene expression and genome structure among relatively 'young' and 'established' or 'ancient' polyploids. Powerful reverse and forward genetics in Arabidopsis offer an exceptional means by which regulatory mechanisms of gene and genome duplication may be revealed. Moreover, the Arabidopsis genome is completely sequenced; both coding and non-coding sequences are available. We have developed spotted oligo-gene and chromosome microarrays using the complete Arabidopsis genome sequence. The oligo-gene microarray consists of ∼26 000 70-mer oligonucleotides that are designed from all annotated genes in Arabidopsis , and the chromosome microarray contains 1 kb genomic tiling fragments amplified from a chromosomal region or the complete sequence of chromosome 4. We have demonstrated the utility of microarrays for genome-wide analysis of changes in gene expression, genome organization and chromatin structure in Arabidopsis polyploids and related species.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 689–700.     

Polyploidy in vertebrate ancestry: Ohno and beyond

Over 30 years ago, Susumu Ohno proposed that two rounds of polyploidy occurred early in vertebrate evolution. We re-examine this proposal using three recent lines of evidence. First, total gene number estimates from completely sequenced genomes suggest an increase in total gene number somewhere along the vertebrate or prevertebrate lineage, compatible with Ohno's model. Second, analyses of homeobox and other genes from amphioxus reveal very extensive gene duplication specifically on the vertebrate lineage. This refines the timing of putative polyploidy to after the divergence of amphioxus and vertebrates. Third, the existence of four-fold paralogy regions in the human genome is suggestive of two rounds of polyploidy, although other explanations are possible. We propose an experimental test, based on chromosomal localization of genes in amphioxus, that should resolve whether paralogy regions are indeed remnants of duplication in vertebrate ancestry.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 425–430.     

Spartina anglica C. E. Hubbard: a natural model system for analysing early evolutionary changes that affect allopolyploid genomes

Spartina anglica arose during the end of the 19th century in England by hybridization between the indigenous Spartina maritima and the introduced East American Spartina alterniflora and following genome duplication of the hybrid ( S.  ×  townsendii ). This system allows investigations of the early evolutionary changes that accompany stabilization of a new allopolyploid species in natural populations. Various molecular data indicate that S. anglica has resulted from a unique parental genotype. This young species contains two distinctly divergent homoeologous genomes that have not undergone extensive change since their reunion. No burst of retroelements has been encountered in the F₁ hybrid or in the allopolyploid, suggesting a 'structural genomic stasis' rather than 'rapid genomic changes'. However, modifications of the methylation patterns in the genomes of S.  ×  townsendii and S. anglica indicate that in this system, epigenetic changes have followed both hybridization and polyploidization.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 475–484.     

Genomic creativity and natural selection: a modern synthesis

In the early 1930s, the synthesis of Darwinian natural selection, mutation, and Mendelian genetics gave rise to the paradigm of 'modern Darwinism', also known as 'neo-Darwinism'. This has contributed greatly to our understanding. But increasing knowledge of other mechanisms, including endosymbiosis, genetic and genomic duplication, polyploidy, hybridization, epigenetics, horizontal gene transfer in prokaryotes, and the modern synthesis of embryonic development and evolution, has widened our horizons to a diversity of possibilities for change. All of these can be gathered under the umbrella concept of 'genomic creativity', which, in partnership with natural selection, affords a more comprehensive modern explanation of evolution.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 655–672.     

Whole-genome duplications in South American desert rodents (Octodontidae)

The discovery of tetraploidy in the red viscacha rat, Tympanoctomys barrerae (4 n  = 102) has emphasized the evolutionary role of genome duplication in mammals. The tetraploid status of this species is corroborated here by in situ PCR and Southern blot analysis of a single-copy gene. The species meiotic configuration strongly suggests a hybrid derivation. To investigate the origin of T. barrerae further, the recently described Pipanacoctomys aureus was studied. This 92-chromosome species also has a duplicated genome size, redundant gene copy number and diploid-like meiotic pairing, consistent with an event of allotetraploidization. Phylogenetic analysis of mitochondrial sequences indicates sister-group relationships between these two tetraploid rodents. The new karyotypic data and the phylogenetic relationships suggest the participation of the ancestral lineages of Octomys mimax in the genesis of P. aureus . The high overall DNA similarity and shared band homology revealed by genomic Southern hybridization as well as matching chromosome numbers between O. mimax and the descendant tetraploid species support the notion of introgressive hybridization between these taxa.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 443–451.     

Incipient speciation driven by phenotypic plasticity? Evidence from sympatric populations of Arctic charr

Recent models suggest that the existence of environmentally induced polymorphisms within a single population (especially those related to foraging) facilitates the process of evolutionary divergence within a single gene pool by generating distinct phenotypic modes that are exposed to differential selection. In order to test a prediction of the phenotypic plasticity model of divergence, we used a well-documented polymorphism to disentangle the relative effects of morph and rearing environment in generating phenotypic variance. We reared first-generation offspring of two sympatric morphs of Arctic charr Salvelinus alpinus in the laboratory and compared their head morphology with that of their wild parents. Morphological characters with a known functional role in foraging were highly plastic. Rearing environment accounted for the largest component of the variation in expressed phenotype, but this environmental effect overlaid a clear (but small) genetic effect. We conclude that phenotypic plasticity has played a significant role in the evolution of this trophic polymorphism, but that the evolutionary process has progressed to the point that the gene pool is now segregated.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 611–618.     

Evolution of South American mammalian predators (Borhyaenoidea): anatomical and palaeobiological implications

The evolution of South American carnivorous marsupials, the borhyaenoids, has been investigated through the functional analysis of postcranial adaptive traits and palaeobiological data. There is evidence that the evolutionary history of Borhyaenoidea proceeded from a noncursorial ancestor. The locomotion and habits of the early Palaeocene Mayulestes ferox probably approached a generalized plesiomorphic pattern for marsupial locomotion, i.e. primarily terrestrial with secondary arboreal adaptations. An exceptionally rich early Miocene Patagonian fauna has yielded various morphological predator types, from scansorial ambusher to terrestrial, incipiently cursorial, taxa. The most specialized borhyaenoid was the powerful sabretooth Thylacosmilus atrox that survived until the late Pliocene. The evolution from a scansorial pattern towards a cursorial trend, illustrated by Borhyaena tuberata , and towards the probable development of postlactational parental care in Thylacosmilus , required by its dental specialization and killing strategy, suggests a modification of the selective pressures and predatory activities of the group over evolutionary time.  © 2004 The Linnean Society of London, Zoological Journal of the Linnean Society , 2004, 140 , 487–521.     

The evolutionary radiation of modern birds (Neornithes): reconciling molecules, morphology and the fossil record

The pattern, timing and extent of the evolutionary radiation of anatomically modern birds (Neornithes) remains contentious: dramatically different timescales for this major event in vertebrate evolution have been recovered by the 'clock-like' modelling of molecular sequence data and from evidence extracted from the known fossil record. Because current synthesis would lead us to believe that fossil and nonfossil evidence conflict with regard to the neornithine timescale, especially at its base, it is high time that available data are reconciled to determine more exactly the evolutionary radiation of modern birds. In this review we highlight current understanding of the early fossil history of Neornithes in conjunction with available phylogenetic resolution for the major extant clades, as well as recent advancements in genetic methods that have constrained time estimates for major evolutionary divergences. Although the use of molecular approaches for timing the radiation of Neornithes is emphasized, the tenet of this review remains the fossil record of the major neornithine subdivisions and better-preserved taxa. Fossils allowing clear phylogenetic constraint of taxa are central to future work in the production of accurate molecular calibrations of the neornithine evolutionary timescale.  © 2004 The Linnean Society of London, Zoological Journal of the Linnean Society , 2004, 141 , 153–177.     

Concerted evolution of 18–5.8–26S rDNA repeats in Nicotiana allotetraploids

We review and extend data showing concerted evolution of parental 18–5.8–26S nuclear ribosomal DNA (18–26S rDNA) gene families in three natural Nicotiana allotetraploids ( N. tabacum , N. rustica and N. arentsii , each 2 n  = 4 x  = 48) and one synthetic N. tabacum line (Th37, ♀ N. sylvestris (2 n  = 24) × ♂ N. tomentosiformis (2 n  = 24)). The origin of the gene families was analysed by sequence polymorphisms in the intergenic spacer (IGS) region and the number of chromosomal loci by fluorescence in situ hybridization (FISH). FISH revealed that the number and locations of 18–26S rDNA in the natural allopolyploids was the sum of those found in the diploid progenitors. However, the rDNA restriction patterns showed polymorphisms in the IGS that were not additive, suggesting that parental rDNA clusters were partially ( N. tabacum, N. rustica ) or completely ( N. arentsii ) overwritten by hybrid-specific units. Thus the Nicotiana allotetraploids show evidence of concerted evolution, including both intralocus and interlocus gene conversion. A feral N. tabacum collected in Bolivia had a higher proportion of unconverted parental rDNA units than cultivated tobacco varieties, suggesting either that rDNA homogenization is accelerated by inbreeding or multiple origins of tobacco. There is no evidence for the elimination of N. sylvestris- derived rDNA units in the synthetic Th37 tobacco line as occurred in natural tobacco, although several novel rDNA unit variants were found in most but not all the hybrid plants. Factors that may control the occurrence and extent of rDNA homogenization are discussed for allopolyploids in Nicotiana and other taxa.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 615–625.     

Stability of genetic structure and effective population size inferred from temporal changes of microsatellite DNA polymorphisms in the land snail Helix aspersa (Gastropoda: Helicidae)

Temporal evolution of genetic variability may have far-reaching consequences for a diverse array of evolutionary processes. Within the polders of the Bay of Mont-Saint-Michel (France), populations of the land snail Helix aspersa are characterized by a metapopulation structure with occasional extinction processes resulting from farming practices. A temporal survey of genetic structure in H . aspersa was carried out using variability at four microsatellite loci, in ten populations sampled two years apart. Levels of within-population genetic variation, as measured by allelic richness, H _e or F _is , did not change over time and similar levels of population differentiation were demonstrated for both sampling years. The extent of genetic differentiation between temporal samples of the same population established (i) a stable structure for six populations, and (ii) substantial genetic changes for four populations. Using classical F -statistics and a maximum likelihood method, estimates of the effective population size ( N _e) illustrated a mixture of stable populations with high N _e, and unstable populations characterized by very small N _e estimates (of 5–11 individuals). Owing to human disturbances, intermittent gene flow and genetic drift are likely to be the predominant evolutionary processes shaping the observed genetic structure. However, the practice of multiple matings and sperm storage is likely to provide a reservoir of variability, minimizing the eroding genetic effects of population size reduction and increasing the effective population size.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 89–102.     

Molecular phylogeny and zoogeography of the freshwater crayfish genus Cherax Erichson (Decapoda: Parastacidae) in Australia

The evolutionary history and biogeography of freshwater-dependent taxa in Australia is of intrinsic interest given the present-day aridity of this continent. Cherax is the most widespread and one of the most species-rich of Australia's nine freshwater crayfish genera. The phylogenetic relationships amongst 19 of the 23 Australian Cherax were established from mitochondrial DNA sequences representing the 12S rRNA and 16S rRNA gene regions. The relationships among species support an initial east–west separation, followed by a north–south divergence in eastern Australia. Molecular clock estimations suggest that these divergences date back to the Miocene. The phylogenetic relationships support endemic speciation within geographical regions and indicate that long-distance dispersal has not led to recent speciation as previously hypothesized. This new evolutionary scenario is consistent with the climatic history of Australia and the evolutionary history of other similarly distributed freshwater-dependent organisms in Australia.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 553–563.     

Genome redundancy and plasticity within ancient and recent Brassica crop species

The crop species within the genus Brassica have highly replicated genomes. Three base 'diploid' species, Brassica oleracea , B. nigra and B. rapa , are likely ancient polyploids, and three derived allopolyploid species, B. carinata , B. juncea and B. napus , are created from the interspecific hybridization of these base genomes. The base Brassica genome is thought to have hexaploid ancestry, and both recent and ancient polyploidization events have been proposed to generate a large number of genome rearrangements and novel genetic variation for important traits. Here, we revisit and refine these hypotheses. We have examined the B. oleracea linkage map using the Arabidopsis thaliana genome sequence as a template and suggest that there is strong evidence for genome replication and rearrangement within the base Brassicas, but less evidence for genome triplication. We show that novel phenotypic variation within the base Brassicas can be achieved by replication of a single gene, BrFLC , that acts additively to influence flowering time. Within the derived allopolyploids, intergenomic heterozygosity is associated with higher seed yields. Some studies have reported that de novo genomic variation occurs within derived polyploid genomes, whereas other studies have not detected these changes. We discuss reasons for these different findings. Large translocations and tetrasomic inheritance can explain some but not all genomic changes within the polyploids. Transpositions and other small-scale sequence changes probably also have contributed to genomic novelty. Our results have shown that the Brassica genomes are remarkably plastic, and that polyploidy generates novel genetic variation through gene duplication, intergenomic heterozygosity and perhaps epigenetic change.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 665–674.     

A tangled history: patterns of major histocompatibility complex evolution in the African mole-rats (Family: Bathyergidae)

Phylogenetic trees based upon major histocompatibility complex (MHC) gene sequences, particularly those encompassing sites encoding the antigen recognition site, are often discordant with the species tree. It has been argued that the principal cause of such discordance is the presence of ancestrally derived polymorphisms persisting through speciation events as a consequence of selection. In the present study, we examine the evolution of the MHC class II DQα1 gene in an unusual family of hystricomorph rodents, the African mole-rats (Family: Bathyergidae). We show that there is a high level of trans-species polymorphism and that this is a result of positive selection. Furthermore, the major lineages of the gene tree are characterized by allelic motifs occurring in regions that coincide with the pocket domains of the putative antigen recognition site, a region that has been shown to be under positive selection in a number of MHC genes from a range of species. Finally, these alleles may have been retained for at least 48 million years. This is significantly older than the estimate for the equivalent primate locus and appears to be one of the oldest documented sets of MHC alleles. We suggest that these allelic motifs possess polymorphisms that have been immunologically important to African mole-rats over long periods of evolutionary history.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 493–503.     

Evolution of the secretoglobins: a genomic and proteomic view

Mouse salivary androgen-binding protein (ABP) is a member of the newly erected secretoglobin family, no member of which has yet been assigned an indisputable function. We have suggested a role for ABP in mate selection behaviour and sexual isolation. Although this has been a particularly attractive hypothesis given the evidence for strong positive selection on its alpha subunit gene, Abpa , we have held out the possibility that there might be an as-yet-undiscovered primary function for ABP. This is particularly important in light of its membership in the secretoglobin family, and we are pursuing the broader issue of shared functions of the secretoglobins with genomic and bioinformatic studies. Here we present as complete a comparison as possible of the secretoglobins in the genomes of three species of mammals: mouse, rat and human, and we compare the protein sequences and their potential evolutionary relationships. We suggest that the secretoglobins can be divided into at least five families. In rodent and human genomes, these gene families are found in two main clusters that are syntenic between rat and mouse. Humans have only the three families that are found within the uteroglobin/clara cluster, because no ABP-containing secretoglobin cluster has yet been identified.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 493–501.     

Plant polyploidy and the evolutionary ecology of plant/animal interactions

Until recently almost nothing was known about the effects of plant polyploidy on interactions with herbivores and pollinators. Studies of the saxifrage Heuchera grossulariifolia throughout its geographical range in the US northern Rockies have shown that autopolyploidy has probably arisen multiple times within this species since the end of the Pleistocene. Tetraploids from those different origins experience higher levels of attack by the moth Greya politella (Prodoxidae) than sympatric or parapatric diploids. In addition, within one intensively studied region, the plants are also attacked by two other lepidopteran species: G. piperella , which preferentially attack diploids, and Eupithecia misturata (Geometridae), which preferentially attacks tetraploids. Sympatric diploid and tetraploid plants also differ in the overall suites of pollinators they attract. Hence, the evolution of polyploid populations has the potential to change significantly the evolutionary ecology of interactions with herbivores and pollinators. Because a large number of plant lineages include polyploid species, the evolution of plant polyploidy may have had major effects on the interaction structure of terrestrial communities.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 511–519.     

Multiple origins of viviparity,or reversal from viviparity to oviparity? The European common lizard (Zootoca vivipara,Lacertidae) and the evolution of parity

The evolution of viviparity in squamates has been the focus of much scientific attention in previous years. In particular, the possibility of the transition from viviparity back to oviparity has been the subject of a vigorous debate. Some studies have suggested this reversal is more frequent than previously thought. However, none of them provide conclusive evidence. We investigated this problem by studying the phylogenetic relationships between oviparous and viviparous lineages of the reproductively bimodal lizard species Zootoca vivipara . Our results show that viviparous populations are not monophyletic, and that several evolutionary transitions in parity mode have occurred. The most parsimonious scenario involves a single origin of viviparity followed by a reversal back to oviparity. This is the first study with a strongly supported phylogenetic framework supporting a transition from viviparity to oviparity.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 1–11.     

Evolution of the perennial soybean polyploid complex (Glycine subgenus Glycine): a study of contrasts

Glycine subgenus Glycine , the sister group to the cultivated soybean and its progenitor, have received considerable study over several decades. The combination of biosystematic data and an extensive germplasm collection has provided a strong foundation for molecular systematic studies in the group, including those on allopolyploids. These studies have shown that the various polyploid taxa known from the subgenus are all part of a single large allopolyploid complex, linked by shared diploid genomes. Many elements of the complex have arisen recently, and most show evidence of recurrent origins. However, there are also many dissimilarities among even closely related polyploids. Polyploids differ from one another in such ways as number of origins, amount of allelic diversity harboured at different loci, bidirectional vs. unidirectional origins, retention of ribosomal gene homoeologues, success as measured by geographical range and abundance, and patterns of gene expression.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 583–597.     

Seed dormancy in relation to seed storage behaviour in Acer

Dormancy in seeds of Acer opalus is shown to be mainly caused by the seed coats, although a slight embryo dormancy exists in fresh seeds. The ability to germinate after drying indicates that seed storage behaviour is orthodox. Recalcitrant seeds were heavier than orthodox seeds not only within section Acer but also within the whole genus after statistical control of phylogeny, through a phylogenetic ANOVA with data from two different Acer phylogenies. An evolutionary change from orthodox to recalcitrant behaviour is postulated for genus Acer , but this change appears not to have been accompanied by a change in seed dormancy, at least in the taxonomic section in which Acer opalus belongs.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 145 , 203–208.