Fitness of Crop-Wild Hybrid Sunflower under Competitive Conditions: Implications for Crop-to-Wild Introgression

Understanding the likelihood and extent of introgression of novel alleles in hybrid zones requires comparison of lifetime fitness of parents and hybrid progeny. However, fitness differences among cross types can vary depending on biotic conditions, thereby influencing introgression patterns. Based on past work, we predicted that increased competition would enhance introgression between cultivated and wild sunflower (Helianthus annuus) by reducing fitness advantages of wild plants. To test this prediction, we established a factorial field experiment in Kansas, USA where we monitored the fitness of four cross types (Wild, F₁, F₂, and BC_w hybrids) under different levels of interspecific and intraspecific competition. Intraspecific manipulations consisted both of density of competitors and of frequency of crop-wild hybrids. We recorded emergence of overwintered seeds, survival to reproduction, and numbers of seeds produced per reproductive plant. We also calculated two compound fitness measures: seeds produced per emerged seedling and seeds produced per planted seed. Cross type and intraspecific competition affected emergence and survival to reproduction, respectively. Further, cross type interacted with competitive treatments to influence all other fitness traits. More intense competition treatments, especially related to density of intraspecific competitors, repeatedly reduced the fitness advantage of wild plants when considering seeds produced per reproductive plant and per emerged seedling, and F₂ plants often became indistinguishable from the wilds. Wild fitness remained superior when seedling emergence was also considered as part of fitness, but the fitness of F₂ hybrids relative to wild plants more than quadrupled with the addition of interspecific competitors and high densities of intraspecific competitors. Meanwhile, contrary to prediction, lower hybrid frequency reduced wild fitness advantage. These results emphasize the importance of taking a full life cycle perspective. Additionally, due to effects of exogenous selection, a given hybrid generation may be especially well-suited to hastening introgression under particular environmental conditions.     

Fitness of reciprocal F1 hybrids between Rhinanthus minor and Rhinanthus major under controlled conditions and in the field

The performance of first‐generation hybrids determines to a large extent the long‐term outcome of hybridization in natural populations. F₁ hybrids can facilitate further gene flow between the two parental species, especially in animal‐pollinated flowering plants. We studied the performance of reciprocal F₁ hybrids between Rhinanthus minor and R. major, two hemiparasitic, annual, self‐compatible plant species, from seed germination to seed production under controlled conditions and in the field. We sowed seeds with known ancestry outdoors before winter and followed the complete life cycle until plant death in July the following season. Germination under laboratory conditions was much lower for the F₁ hybrid formed on R. major compared with the reciprocal hybrid formed on R. minor, and this confirmed previous results from similar experiments. However, this difference was not found under field conditions, which seems to indicate that the experimental conditions used for germination in the laboratory are not representative for the germination behaviour of the hybrids under more natural conditions. The earlier interpretation that F₁ hybrid seeds formed on R. major face intrinsic genetic incompatibilities therefore appears to be incorrect. Both F₁ hybrids performed at least as well as and sometimes better than R. minor, which had a higher fitness than R. major in one of the two years in the greenhouse and in the field transplant experiment. The high fitness of the F₁ hybrids confirms findings from naturally mixed populations, where F₁ hybrids appear in the first year after the two species meet, which leads to extensive advanced‐hybrid formation and introgression in subsequent generations.     

The role of seed traits as segregation factors of hybrids in wild populations of Cistus (Cistaceae)

Hybridization has been postulated as a main speciation mechanism in Cistus, a hard-seeded group of plants widely distributed in fire-prone Mediterranean shrublands. However, ecological evidence about how the segregation of hybrids from parents might occur is nonexistent. The presence of two hybrid populations in Morocco and Spain from Cistus albidus and Cistus heterophyllus led us to investigate their seed trait differences (seed size, mass and coat thickness) with the parentals and their seed germinability. A sowing experiment to compare the seedling emergence ability and seedling fitness of hybrids and their parentals was also carried out. Hybrid seeds germinated in a similar proportion to those of the parents. The hybrid seeds were significantly lighter, smaller and had thinner seed coats in both populations. However, these seed trait differences did not affect the seedling fitness of hybrids. These results were interpreted as a successful shift in the regeneration niche of the hybrids due to a greater proportion of soft-coated seeds, able to emerge from the soil seed bank in absence of fire. Smaller seeds also would favour further and deeper seed dispersal to escape from a fire. Monitoring of the seed yield of the Spanish population showed a competitive ability of hybrids.     

Airborne‐pollen pool and mating pattern in a hybrid zone between Pinus pumila and P. parviflora var. pentaphylla

The reproductive isolation barriers and the mating patterns among Pinus pumila, P. parviflora var. pentaphylla and their hybrids were examined by flowering phenology and genetic assays of three life stages: airborne‐pollen grains, adults and seeds, in a hybrid zone on Mount Apoi, Hokkaido, Japan. Chloroplast DNA composition of the airborne‐pollen was determined by single‐pollen polymerase chain reaction. Mating patterns were analysed by estimating the molecular hybrid index of the seed parent, their seed embryos and pollen parents. The observation of flowering phenology showed that the flowering of P. pumila precedes that of P. parviflora var. pentaphylla by about 6 to 10 days within the same altitudinal ranges. Although this prezygotic isolation barrier is effective, the genetic assay of airborne‐pollen showed that the two pine species, particularly P. pumila, still have chances to form F₁ hybrid seeds. Both parental species showed a strong assortative mating pattern; F₁ seeds were found in only 1.4% of seeds from P. pumila mother trees and not at all in P. parviflora var. pentaphylla. The assortative mating was concluded as the combined result of flowering time differentiation and cross‐incompatibility. In contrast to the parental species, hybrids were fertilized evenly by the two parental species and themselves. The breakdown of prezygotic barriers (intermediate flowering phenology) and cross‐incompatibility may account for the unselective mating. It is suggested that introgression is ongoing on Mount Apoi through backcrossing between hybrids and parental species, despite strong isolation barriers between the parental species.     

Clarification of the genetic component of hybrids between Phyllodoce caerulea and Phyllodoce aleutica (Ericaceae) in Hokkaido,northern Japan

Natural hybridization provides great opportunities to understand the interaction of genetics and ecology in determining species boundaries. We examined the genetic relationships of Phyllodoce taxa and revealed that most hybrids were fertile F₁s and an extremely small number of backcross and no F₂ plants were established in natural conditions. Because this trend was irrespective of regions, we conclude that negative endogenous selection may act after the germination of F₁ seeds and prevent the establishment of later‐generation hybrids. Based on these results, we discuss the ecological and evolutionary significance of natural hybridization in Phyllodoce taxa.     

HYBRID FITNESS IN THE LOUISIANA IRISES: ANALYSIS OF PARENTAL AND F1 PERFORMANCE

The assumption of hybrid inferiority is central to the two models most widely applied to the prediction of hybrid zone evolution. Both the tension zone and mosaic models assume that natural selection acts against hybrids regardless of the environment in which they occur. To test this assumption, we investigated components of fitness in Iris fulva, I. hexagona and their reciprocal F₁ hybrids under greenhouse conditions. The four cross types were compared on the basis of seed germination, vegetative and clonal growth, and sexual reproduction. In all cases, the hybrids performed as well as, or significantly better than, both of their parents. These results suggest that F₁ hybrids between I. fulva and I. hexagona are at least as fit as their parents. The results of this study are therefore inconsistent with the assumptions of both the tension zone and mosaic models of hybrid zone evolution.     

Exogenous selection rather than cytonuclear incompatibilities shapes asymmetrical fitness of reciprocal Arabidopsis hybrids

Reciprocal crosses between species often display an asymmetry in the fitness of F₁ hybrids. This pattern, referred to as isolation asymmetry or Darwin's corollary to Haldane's rule, is a general feature of reproductive isolation in plants, yet factors determining its magnitude and direction remain unclear. We evaluated reciprocal species crosses between two naturally hybridizing diploid species of Arabidopsis to assess the degree of isolation asymmetry at different postmating life stages. We found that pollen from Arabidopsis arenosa will usually fertilize ovules from Arabidopsis lyrata; the reverse receptivity being less complete. Maternal A. lyrata parents set more F₁ hybrid seed, but germinate at lower frequency, reversing the asymmetry. As predicted by theory, A. lyrata (the maternal parent with lower seed viability in crosses) exhibited accelerated chloroplast evolution, indicating that cytonuclear incompatibilities may play a role in reproductive isolation. However, this direction of asymmetrical reproductive isolation is not replicated in natural suture zones, where delayed hybrid breakdown of fertility at later developmental stages, or later‐acting selection against A. arenosa maternal hybrids (unrelated to hybrid fertility, e.g., substrate adaptation) may be responsible for an excess of A. lyrata maternal hybrids. Exogenous selection rather than cytonuclear incompatibilities thus shapes the asymmetrical postmating isolation in nature.     

Genetic structure of a hybrid zone between two violets,Viola rossii Hemsl. and V. bissetii Maxim.: dominance of F1 individuals in a narrow contact range

The genetic composition of a hybrid zone can provide insight into the evolution of diversification in plants. We carried out morphological and amplified fragment length polymorphism analyses to investigate the genetic composition of a hybrid zone between two violets, Viola bissetii Hemsl. and Viola rossii Maxim. Our aim was to clarify the formation and maintenance of hybrids between these Viola species. We found that most hybrid individuals (V. bissetii × V. rossii) were of the F₁ generation, with a few of the F₂ generation. We found no backcrosses. The scarcity of post‐F₁ hybrids indicates that a species barrier is established between the parental species. The F₁‐dominated hybrid zone occupied only a narrow, intermediate ecotone between the parental habitats, suggesting that selection by environmental factors against hybrids may help to maintain the current conditions in this hybrid zone.     

Effect of sire population on the genetic diversity and fitness of F1 progeny in the endangered Chinese endemic Sinocalycanthus chinensis

Sinocalycanthus chinensis Cheng et S. Y. Chang (Calycanthaceae), which has a unique systematic status, is listed as a national second‐class protected plant of China. In this study, the genetic diversity, performance, and fitness of F1 progeny from crosses between the Damingshan (DMS) population of S. chinensis and pollen parents from the Daleishan (DLS) and Longxushan (LXS) populations were examined. The DLS population has a relatively small population size, low genetic diversity, and considerable geographical and genetic distances from the DMS population relative to the LXS population. Compared with naturally occurring seeds, DLS‐sired seeds had the highest thousand‐seed weight, starch content, fat content, germination rate, germination index, and emergence rate, but the lowest protein content. Naturally occurring, open‐pollinated seeds had the lowest thousand‐seed weight, starch content, and fat content, but the highest protein content. Compared with natural F1 progeny, DMS × DLS seedlings had the highest genetic diversity, photosynthetic parameters, and growth characteristics, except for leaf mass ratio and stem mass ratio. Under strong light, DMS × DLS seedlings exhibited a F_v/F_m value of 0.75, while the other two seedling types exhibited F_v/F_m values of 0.65. DLS‐sired seeds had the most vigorous growth characteristics except for leaf mass ratio and stem mass ratio. These results suggest that genetic rescue by transplanting seedlings from the DLS population or hand pollination with pollen from the DLS population would be effective methods to reduce inbreeding depression and obtain strong offspring with high genetic diversity and fitness in the DMS population.     

Increased pre-dispersal seed predation in sunflower crop-wild hybrids

The fitness of crop-wild hybrids can influence gene flow between crop and wild populations. Seed predation levels in crop-wild hybrid plants can be an important factor in determining plant fitness, especially in large-seeded crops such as sunflower. To determine patterns of pre-dispersal seed predation, seeds were collected from wild sunflowers (Helianthus annuus L.) and wild×crop F₁ hybrids at three experimental field sites in eastern Kansas. Seed heads were dissected and each seed was counted and scored for categories of seed damage by lepidopteran and coleopteran larvae. Hybrid seed heads showed significantly higher levels of insect-damaged seeds. The average hybrid plant had 36.5% of its seeds (or 45.1 seeds per plant) eaten by insect larvae while the average wild plant lost only 1.8% (or 95 seeds) to seed predators. Hybrid populations had higher levels of total insect damage even when date of flowering, flower head diameter, and the number of open heads within the study site were accounted for. These results suggest that the reduced fecundity of F₁ crop-wild sunflower hybrids demonstrated in other studies may be augmented by the increased seed predation in hybrid flower heads. Fecundity estimates of crop-wild hybrid and wild plants that disregard differential seed predation levels may not accurately reflect the actual relative contributions of hybrid and wild plants to future generations. Received: 21 December 1998 / Accepted: 8 July 1999     

Diagnostic SNPs reveal widespread introgressive hybridization between introduced bighead and silver carp in the Mississippi River Basin

Hybridization among conspecifics in native and introduced habitats has important implications for biological invasions in new ecosystems. Bighead (Hypophthalmichthys nobilis) and silver carp (H. molitrix) are genetically isolated and occur in sympatry within their native range. Following their introduction to North America, however, introgressant hybrids have been reported throughout their expanded range within the Mississippi River Basin (MRB). The extent of introgression, both spatially and generationally, is largely unknown. Therefore, we examined mixed‐species populations from across the MRB to characterize the extent of interspecific gene flow. We assayed 2798 individuals from nine locations with a suite of species‐diagnostic SNPs (57 nuclear and one mitochondrial). Forty‐four per cent (n = 1244) of individuals displayed hybrid genotypes. Moreover, the composition of hybrid genotypes varied among locations and represented complex hybrid swarms with multiple generations of gene flow. Introgressive hybrids were identified from all locations, were bidirectional and followed a bimodal distribution consisting primarily of parental or parental‐like genotypes and phenotypes. All described hybrid categories were present among individuals from 1999 to 2008, with parents and later‐generation backcrosses representing the largest proportion of individuals among years. Our mitochondrial SNP (COII), tested on a subset of 730 individuals, revealed a silver carp maternal bias in 13 of 21 (62%) F₁ hybrids, in all silver carp backcrosses, and maintained throughout many of the bighead carp backcrosses. The application of this suite of diagnostic markers and the spatial coverage permits a deeper examination of the complexity in hybrid swarms between two invasive, introduced species.     

QTL affecting fitness of hybrids between wild and cultivated soybeans in experimental fields

The objective of this study was to identify quantitative trait loci (QTL) affecting fitness of hybrids between wild soybean (Glycine soja) and cultivated soybean (Glycine max). Seed dormancy and seed number, both of which are important for fitness, were evaluated by testing artificial hybrids of G. soja × G. max in a multiple‐site field trial. Generally, the fitness of the F₁ hybrids and hybrid derivatives from self‐pollination was lower than that of G. soja due to loss of seed dormancy, whereas the fitness of hybrid derivatives with higher proportions of G. soja genetic background was comparable with that of G. soja. These differences were genetically dissected into QTL for each population. Three QTLs for seed dormancy and one QTL for total seed number were detected in the F₂ progenies of two diverse cross combinations. At those four QTLs, the G. max alleles reduced seed number and severely reduced seed survival during the winter, suggesting that major genes acquired during soybean adaptation to cultivation have a selective disadvantage in natural habitats. In progenies with a higher proportion of G. soja genetic background, the genetic effects of the G. max alleles were not expressed as phenotypes because the G. soja alleles were dominant over the G. max alleles. Considering the highly inbreeding nature of these species, most hybrid derivatives would disappear quickly in early self‐pollinating generations in natural habitats because of the low fitness of plants carrying G. max alleles.     

超甜玉米种子萌发物质利用性状杂种优势及亲子回归关系分析

为阐明超甜玉米(Zea mays L.var.saccharata Bailey)亲本对F_1种子物质利用性状遗传效应,研究了19份自交系和其测配的10个杂交组合的杂种优势及亲子回归关系。结果表明,超甜玉米自交系及F_1种子的淀粉含量、蛋白质含量、脂肪含量、百粒重、种子物质动用量和种子物质利用率差异较大,10个杂交组合中亲本和F_1种子的淀粉含量、脂肪含量、百粒重均存在显著差异。F_1种子淀粉含量和百粒重均表现出正向超亲优势,即近高亲本遗传;而F_1种子的蛋白质含量、脂肪含量、种子物质动用量和种子物质利用率为近低亲本遗传。聚类分析和杂种优势分析表明,性状差异较大的FH14、Q26、GT22、GT2等亲本测配的杂交组合在种子百粒重或种子物质利用率等性状上具有较强的超亲优势。回归分析表明,母本对F_1种子的淀粉含量、百粒重有负效应,对种子物质动用量和种子物质利用率有正效应;父本对种子淀粉含量有负效应,对种子物质利用率有正效应。     

Wide hybridization in Brassica

Summary Crosses were made to obtain interspecific hybrids between B. fruticulosa (wild species , 2n = 16) × B. campestris (cultivar , 2n = 20). Although many pollen grains germinated and their tubes entered the style, only about 30% of the ovules received pollen tubes. Fertilized ovules aborted at various stages of development. A few hybrid seeds resulted from hand pollinations in the field, and they showed poor germination and seedling establishment. The in vitro culture of ovaries, ovules, and seeds increased the frequency of obtaining hybrid seeds and plants: the most effective method was ovary culture followed by ovule culture. The hybrid nature of the plants was confirmed through morphological, cytological, and electrophoretic studies. A meiotic analysis of F₁ hybrids (2n = 18) showed that they had 0–5 bivalents and were completely pollen sterile. Electrophoretic analysis of leaf esterases and acid phosphatases of F₁ hybrids revealed bands derived from each parent. Induced amphidiploids of F₁ hybrids contained mostly bivalents, and had about 50% fertile pollen.     

GENETIC ARCHITECTURE OF ISOLATION BETWEEN TWO SPECIES OF SILENE WITH SEX CHROMOSOMES AND HALDANE'S RULE

Examination of the genetic architecture of hybrid breakdown can provide insight into the genetic mechanisms of commonly observed isolating phenomena such as Haldane's rule. We used line‐cross analysis to dissect the genetic architecture of divergence between two plant species that exhibit Haldane's rule for male sterility and rarity, Silene latifolia and Silene diclinis. We made 15 types of crosses, including reciprocal F₁, F₂, backcrosses, and later‐generation crosses, grew the seeds to flowering, and measured the number of viable ovules, proportion of viable pollen, and sex ratio. Typically, Haldane's rule for male rarity in XY animal hybrids is explained by interactions involving recessive X‐linked alleles that are deleterious when hemizygous (dominance theory), whereas sterility is explained by rapid evolution of spermatogenesis genes (faster‐male evolution). In contrast, we found that the genetic mechanisms underlying Haldane's rule between the two Silene species did not follow these conventions. Dominance theory was sufficient to explain male sterility, but male rarity likely involved faster‐male evolution. We also found an effect of the neo‐sex chromosomes of S. diclinis on the extreme rarity of some hybrid males. Our findings suggest that the genetic architecture of Haldane's rule in dioecious plants may differ from those commonly found in animals.     

Hierarchical behaviour,habitat use and species size differences shape evolutionary outcomes of hybridization in a coral reef fish

Hybridization is an important evolutionary process, with ecological and behavioural factors influencing gene exchange between hybrids and parent species. Patterns of hybridization in anemonefishes may result from living in highly specialized habitats and breeding status regulated by size‐based hierarchal social groups. Here, morphological, ecological and genetic analyses in Kimbe Bay, Papua New Guinea, examine the hybrid status of Amphiprion leucokranos, a nominal species and presumed hybrid between Amphiprion sandaracinos and Amphiprion chrysopterus. We test the hypothesis that habitat use and relative size differences of the parent species and hybrids determine the patterns of gene exchange. There is strong evidence that A. leucokranos is a hybrid of smaller A. sandaracinos and larger A. chrysopterus, where A. chrysopterus is exclusively the mother to each hybrid, based on mtDNA cytochrome b and multiple nDNA microsatellite loci. Overlap in habitat, depth and host anemone use was found, with hybrids intermediate to parents and cohabitation in over 25% of anemones sampled. Hybrids, intermediate in body size, colour and pattern, were classified 55% of the time as morphologically first‐generation hybrids relative to parents, whereas 45% of hybrids were more A. sandaracinos‐like, suggesting backcrossing. Unidirectional introgression of A. chrysopterus mtDNA into A. sandaracinos via hybrid backcrosses was found, with larger female hybrids and small male A. sandaracinos mating. Potential nDNA introgression was also evident through distinct intermediate hybrid genotypes penetrating both parent species. Findings support the hypothesis that anemonefish hierarchical behaviour, habitat use and species‐specific size differences determine how hybrids form and the evolutionary consequences of hybridization.     

Morphometric and population genetic analyses elucidate the origin,evolutionary significance and conservation implications of Orchis × angusticruris (O. purpurea × O. simia), a hybrid orchid new to Britain

We report the first confirmed occurrence in Britain of Orchis × angusticruris Franch. ex Rouy, a hybrid between two closely related orchid species of anthropomorphic Orchis (O. purpurea Huds. × O. simia Lam.) that hybridize frequently in Continental Europe. Seven individual hybrids, most likely F1 plants representing a single interspecific pollination event, first flowered with both parents in May 2006 at a nature reserve in the Chiltern Hills near Goring, Oxfordshire. Univariate and multivariate morphometric analyses (43 characters plus 12 indices), internal transcribed spacer sequencing, plastid microsatellites and amplified fragment length polymorphism (AFLP) analyses together readily separate the parents and confirm that O. purpurea was the ovule parent and O. simia the pollen parent, presumably reflecting the greater frequency and/or later flowering period of the latter at the site. This study reinforces a more general observation that, in most orchids, the ovule parent contributes substantially more to the hybrid phenotype than does the pollen parent, perhaps reflecting cytoplasmic inheritance. In contrast, the hybrids are placed closer to O. simia than to O. purpurea in the AFLP tree. Apparently recent arrivals, the few O. purpurea plants at Goring contrast genetically with the two other small populations of this species known in the Chilterns, but rather are consistent with relatively uncommon Continental populations. This suggests that the plants may have been deliberately introduced at Goring by man, although transport from the Continent in high‐level air currents cannot be ruled out. The Goring population of O. simia is likely to have become genetically impoverished through (1) preferential removal of many relatively fit plants to herbaria in the 19^th century and/or (2) a catastrophic population crash in the first half of the 20^th century. However, both our re‐examination of herbarium specimens and our population genetic data indicate past hybridization among anthropomorphic Orchis species occurring naturally in the Chilterns. Thus, we tentatively recommend retention of the hybrid plants at Goring, despite their likely anthropogenic origin from Continental material and the partial viability of their pollen and seeds, which offers opportunities for future introgression. Although the Goring hybrids broadly resemble morphologically O. militaris, another anthropomorphic Orchis still found at two Chiltern localities, sufficient morphological and molecular differences were observed to strongly refute our initial hypothesis that O. militaris could have originated through hybridization between ancestors that resembled O. purpurea and O. simia. The comparatively complex genetic properties evident in both O. simia and O. purpurea merit further study. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 157 , 687–711.     

Heterosis in hybrids within and between yeast species

The performance of hybrids relative to their parents is an important factor in speciation research. We measured the growth of 46 Saccharomyces yeast F1 interspecific and intraspecific hybrids, relative to the growth of each of their parents, in pairwise competition assays. We found that the growth of a hybrid relative to the average of its parents, a measure of mid‐parent heterosis, correlated with the difference in parental growth relative to their hybrid, a measure of phenotypic divergence, which is consistent with simple complementation of low fitness alleles in one parent by high fitness alleles in the other. Interspecific hybrids showed stronger heterosis than intraspecific hybrids. To manipulate parental phenotypic divergence independently of genotype, we also measured the competitive growth of a single interspecific hybrid relative to its parents in 12 different environments. In these assays, we not only identified a strong relationship between parental phenotypic divergence and mid‐parent heterosis as before, but, more tentatively, a weak relationship between phenotypic divergence and best‐parent heterosis, suggesting that complementation of deleterious mutations was not the sole cause of interspecific heterosis. Our results show that mating between different species can be beneficial, and demonstrate that competition assays between parents and offspring are a useful way to study the evolutionary consequences of hybridization.