Cryptic Trysts, Genomic Mergers, and Plant Speciation

It has long been recognized that interspecific hybridization is common in plants, enhancing processes of diversification and speciation. With the widespread utilization of molecular tools, interspecific hybridization – as revealed through incongruence among two or more phylogenetic data sets – is now inferred to be even more prevalent than indicated by morphological and cytogenetic evidence. UsingGossypium as an example, we show how multiple molecular markers have implicated a high frequency of historical hybridization between lineages whose modern descendants are strongly isolated by geography and intrinsic genetic barriers. For example, transoceanic dispersal of propagules from Africa to the New World led to the creation of a novel allotetraploid lineage, as well as the introgression of African repetitive elements into a Mexican diploid species. By mechanisms that remain obscure, fully one-quarter of modern Gossypiumspecies appear to have experienced historical interspecific cytoplasmic and possibly nuclear introgression. These remarkable observations of interspecific genetic exchange emerge from a genus for which such contact would appear improbable, implying that historical hybridization is a more creative force than suspected in angiosperm evolution

Allozyme Diversity and lntrogression in the Galapagos Islands Endemic Gossypium datwinii and its Relationship to Continental G. barbadense

Gossypium darwinii Watt is a tetraploid cotton endemic to the Galapagos Islands. Opinion has been divided as to whether or not it deserves recognition at the specific rank, with some considering it a variety of its presumed progenitor, the widely distributed South American species G. barbadense L. A previous hypothesis states that much of the perceived intergradation between the two taxa arose as a consequence of introgression from G. barbadense following its introduction to the archipelago during the past several hundred years. We performed allozyme analysis on 58 accessions of G. darwinii from six islands, using 17 enzymes collectively encoded by 59 loci. Levels of variation were high for an island endemic, with a mean number of alleles per locus of 1.34 and an average panmictic heterozygosity of 0.062. Principal component analysis revealed clustering of accessions according to their island of origin, and a spatial pattern of island-clusters that approximates geographical relationships among islands. Genetic relationships of G. darwinii with G. barbadense and G. hirsutum L. were studied using previously generated allozyme data. Significant introgression of G. hirsutum alleles was detected; however morphological considerations support the hypothesis that much of G. darwinii\u27s diversity stems from interspecific gene flow from G. barbadense, Evidence is presented suggesting that the occurrence of G. hirsutum alleles in G. darwinii derives not from direct hybridization, but from a mediated transfer through introduced, G. hirsutum-introgressed;G. barbadense. Gossypium darwinii and G. barbadense are nearly fixed for different alleles at four loci and each contains a large number of unique alleles. Notwithstanding the high interspecific Nei\u27s genetic identity (0.949), the allozyme data support geographical and morphological evidence in suggesting that a specific rank for G. darwinii is warranted

lntrogression and Its Consequences in Plants

The role of introgression in plant evolution has been the subject of considerable discussion since the publication of Anderson\u27s influential monograph, Introgressive Hybridization (Anderson, 1949). Anderson promoted the view, since widely held by botanists, that interspecific transfer of genes is a potent evolutionary force. He suggested that the raw material for evolution brought about by introgression must greatly exceed the new genes produced directly by mutation ( 1949, p. 102) and reasoned, as have many subsequent authors, that the resulting increases in genetic diversity and number of genetic combinations promote the development or acquisition of novel adaptations (Anderson, 1949, 1953; Stebbins, 1959; Rattenbury, 1962; Lewontin and Birch, 1966; Raven, 1976; Grant, 1981 ). In contrast to this adaptationist perspective, others have accorded little evolutionary significance to introgression, suggesting instead that it should be considered a primarily local phenomenon with only transient effects, a kind of evolutionary noise (Barber and Jackson, 1957; Randolph et al., 1967; Wagner, 1969, 1970; Hardin, 1975). One of the vociferous doubters of a significant role of hybridization in plant evolution was Wagner ( 1969, p. 785), who commented that the ultimate contributions made by hybrids must be very small or negligible. Wagner\u27s frequently expressed opinion appears to be based on ecological and compatibility arguments, which were encapsulated as follows: In the rare cases that two well differentiated species happen to be interfertile enough to produce fertile progeny, their hybrids will usually have to fit into some hybrid niche. Such fertile hybrids will therefore tend to be transient, disappearing once the differentiated community returns and the parental species re-occupy their normal habitats

Crop Plants as Models for Understanding Plant Adaptation and Diversification

Since the time of Darwin, biologists have understood the promise of crop plants and their wild relatives for providing insight into the mechanisms of phenotypic evolution. The intense selection imposed by our ancestors during plant domestication and subsequent crop improvement has generated remarkable transformations of plant phenotypes. Unlike evolution in natural settings, descendent and antecedent conditions for crop plants are often both extant, providing opportunities for direct comparisons through crossing and other experimental approaches. Moreover, since domestication has repeatedly generated a suite of domestication syndrome traits that are shared among crops, opportunities exist for gaining insight into the genetic and developmental mechanisms that underlie parallel adaptive evolution. Advances in our understanding of the genetic architecture of domestication-related traits have emerged from combining powerful molecular technologies with advanced experimental designs, including nested association mapping, genome-wide association studies, population genetic screens for signatures of selection, and candidate gene approaches. These studies may be combined with high-throughput evaluations of the various omics involved in trait transformation, revealing a diversity of underlying causative mutations affecting phenotypes and their downstream propagation through biological networks. We summarize the state of our knowledge of the mutational spectrum that generates phenotypic novelty in domesticated plant species, and our current understanding of how domestication can reshape gene expression networks and emergent phenotypes. An exploration of traits that have been subject to similar selective pressures across crops (e.g., flowering time) suggests that a diversity of targeted genes and causative mutational changes can underlie parallel adaptation in the context of crop evolution

Cis–trans controls and regulatory novelty accompanying allopolyploidization

Allopolyploidy is a prevalent process in plants, having important physiological, ecological, and evolutionary consequences. Transcriptomic responses to genomic merger and doubling have been demonstrated in many allopolyploid systems, encompassing a diversity of phenomena including homoeolog expression bias, genome dominance, expression‐level dominance, and revamping of co‐expression networks. Notwithstanding the foregoing, there remains a need to develop a conceptual framework that will stimulate a deeper understanding of these diverse phenomena and their mechanistic interrelationships. Here we introduce considerations relevant to this framework with a focus on cis–trans interactions among duplicated genes and alleles in hybrids and allopolyploids. By extending classic allele‐specific expression analysis to the allopolyploid level, we distinguish the distinct effects of progenitor regulatory interactions from the novel intergenomic interactions that arise from genome merger and allopolyploidization. This perspective informs experiments designed to reveal the molecular genetic basis of gene regulatory control, and will facilitate the disentangling of genetic from epigenetic and higher‐order effects that impact gene expression. Finally, we suggest that the extended cis–trans model may help conceptually unify several presently disparate hallmarks of allopolyploid evolution, including genome‐wide expression dominance and biased fractionation, and lead to a new level of understanding of phenotypic novelty accompanying polyploidy

Recent Insights into Mechanisms of Genome Size Change in Plants

Genome sizes vary considerably across all eukaryotes and even among closely related species. The genesis and evolutionary dynamics of that variation have generated considerable interest, as have the patterns of variation themselves. Here we review recent developments in our understanding of genome size evolution in plants, drawing attention to the higher order processes that can influence the mechanisms generating changing genome size

Molecular Divergence in the Galapagos Islands—Baja California Species Pair, Gossypium klotzschianum and G. davidsonii (Malvaceae)

Molecular divergence betweenGossypium klotzschianum andG. davidsonii was studied. The former is endemic to five of the larger islands of the Galapagos, whileG. davidsonii is restricted to the southern half of Baja California, approximately 2 500 km distant. A substantial body of genetic and taxonomic data suggests that these two species are related as progenitor and derivative. Interspecific hybrids are fully fertile, with no evidence of F2 breakdown and normal segregation of genetic markers. Allozyme analysis of 33 populations for 41 loci indicated that the allelic composition ofG. klotzschianum represents a subset ofG. davidsonii. Although genetic diversity is relatively restricted in both species, calculated measures demonstrate higher levels of genetic variability and greater population structuring inG. davidsonii than inG. klotzschianum. The interspecific genetic identity of 0.87 is typical for progenitor-derivative species pairs. Chloroplast DNAs were surveyed for variation with 25 restriction enzymes using hybridization probes that cover the entire chloroplast genome. No intraspecific and little interspecific variation was detected among 560 cpDNA restriction sites, representing sequence information for approximately 3200 nucleotides. Only 3 mutational differences distinguished the two species, resulting in a sequence divergence estimate of 0.09%. Divergence times were estimated from both the isozyme data and the cpDNA restriction site data. Although these estimates have several sources of error, both molecular data sets were congruent in suggesting that the two lineages diverged between 250000 and 700000 years ago. Accumulated evidence suggests that dispersal was from Baja California to the Galapagos Islands rather than the reverse, and most likely was mediated by trans-oceanic drift.G. klotzschianum may be the only species of the endemic Galapagos flora to have arisen from a northern Mexican progenitor

A New Isozyme Marker for the Short Arm of Chromosome 6

Wendel et al. (MNL 60:109-110) reported isozyme segregation data that suggested Adkl (adenylate kinase) is located near the centromere on chromosome 6, and tentatively proposed a location on 6S. Subsequent work has confirmed that Adkl is on 6S, which is significant in that this is one of the most poorly mapped chromosome arms of maize

Allozyme Evidence for the Origin and Diversification of Gossypium barbadense L.

Gossypium barbadense L. is a commercially important cotton species of tropical South American origin presently grownin many regions of the world. The species is morphologically diverse, consisting of a wide range of wild (or feral), commensal, landrace, and highly improvedcommercial forms. We performed allozyme analysis on 153 accessions representing the spectrum of G. barbadense diversityto ascertain the geographic origin of the species, its patterns of diffusion subsequent to domestication, and to reveal infraspecific relationships. Levels ofgenetic variation in G. barbadense are moderate. Of 59 loci scored, 24 were polymorphic, with a mean number of alleles perlocus of 1.69 and an average panmictic heterozygosity of 0.062. Principal component analysis revealed geographic clustering of accessions into six relativelydiscrete regions. Gene frequencies at many loci are significantly heterogeneous among these regions, with an average G STof 0.272. Northwestern South America contains the greatest genetic variability; we suggest that this region is the ancestral home of the species. The data indicate separate diffusion pathways from this region into Argentina-Paraguay and into eastern and northern South America east of the Andes. Caribbean Island and Central American forms appear to be derived from the latter. These diffusion pathways are in accordance with morphological evidence and historical record. In contrast to expectations based on geographic proximity, Pacific Island forms have their closest affinity to accessions from eastern South America. Advanced cultivated stocks seem largely derived from western Andean material, but also contain introgressed G. hirsutum germ plasm. Introgression was relatively high (22%-50% of accessions) in commercial stocks and in forms from Argentina-Paraguay and various Pacific Islands, but was conspicuously low or absent in material from Central America and the Caribbean, where commensal and commercial forms of both species are sympatric

Comparative Evolutionary and Developmental Dynamics of the Cotton (Gossypium hirsutum) Fiber Transcriptome

The single-celled cotton (Gossypium hirsutum) fiber provides an excellent model to investigate how human selection affects phenotypic evolution. To gain insight into the evolutionary genomics of cotton domestication, we conducted comparative transcriptome profiling of developing cotton fibers using RNA-Seq. Analysis of single-celled fiber transcriptomes from four wild and five domesticated accessions from two developmental time points revealed that at least one-third and likely onehalf of the genes in the genome are expressed at any one stage during cotton fiber development. Among these, ,5,000 genes are differentially expressed during primary and secondary cell wall synthesis between wild and domesticated cottons, with a biased distribution among chromosomes. Transcriptome data implicate a number of biological processes affected by human selection, and suggest that the domestication process has prolonged the duration of fiber elongation in modern cultivated forms. Functional analysis suggested that wild cottons allocate greater resources to stress response pathways, while domestication led to reprogrammed resource allocation toward increased fiber growth, possibly through modulating stress-response networks. This first global transcriptomic analysis using multiple accessions of wild and domesticated cottons is an important step toward a more comprehensive systems perspective on cotton fiber evolution. The understanding that human selection over the past 5,000+ years has dramatically re-wired the cotton fiber transcriptome sets the stage for a deeper understanding of the genetic architecture underlying cotton fiber synthesis and phenotypic evolution