For a new diploid or homoploid hybrid species to become established, it must diverge ecologically from parental genotypes. Otherwise the hybrid neospecies will be overcome by gene flow or competition. We initiated a series of experiments designed to understand how the homoploid hybrid species, Helianthus paradoxus, was able to colonize salt marsh habitats, when both of its parental species (H. annuusxH. petiolaris) are salt sensitive. Here, we report on the results of a quantitative trait locus (QTL) analysis of mineral ion uptake traits and survivorship in 172 BC2 hybrids between H. annuus and H. petiolaris that were planted in H. paradoxus salt marsh habitat in New Mexico. A total of 14 QTLs were detected for mineral ion uptake traits and three for survivorship. Several mineral ion QTLs mapped to the same position as the survivorship QTLs, confirming previous studies, which indicated that salt tolerance in Helianthus is achieved through increased Ca uptake, coupled with greater exclusion of Na and related mineral ions. Of greater general significance was the observation that QTLs with effects in opposing directions were found for survivorship and for all mineral ion uptake traits with more than one detected QTL. This genetic architecture provides an ideal substrate for rapid ecological divergence in hybrid neospecies and offers a simple explanation for the colonization of salt marsh habitats by H. paradoxus. Finally, selection coefficients of +0.126, -0.084 and -0.094 for the three survivorship QTLs, respectively, are sufficiently large to account for establishment of new, homoploid hybrid species.
Diploid hybrid speciation in plants is often accompanied by rapid ecological divergence between incipient neospecies and their parental taxa. One plausible means by which novel adaptation in hybrid lineages may arise is transgressive segregation, that is, the generation of extreme phenotypes that exceed those of the parental lines. Early generation (BC2) hybrids between two wild, annual sunflowers, Helianthus annuus and Helianthus petiolaris, were used to study directional selection on transgressive characters associated with the origin of Helianthus paradoxus, a diploid hybrid species adapted to extremely saline marshes. The BC2 plants descended from a single F1 hybrid backcrossed toward H. petiolaris. The strength of selection on candidate adaptive traits in the interspecific BC2 was measured in natural H. paradoxus salt marsh habitat. Positive directional selection was detected for leaf succulence and Ca uptake, two traits that are known to be important in salt stress response in plants. Strong negative directional selection operated on uptake of Na and correlated elements. A significant decrease in trait correlations over time was observed in the BC2 population for Na and Ca content, suggesting an adaptive role for increased Ca uptake coupled with increased net exclusion of Na from leaves. Patterns of directional selection in BC2 hybrids were concordant with character expression in the natural hybrid species, H. paradoxus, transplanted into the wild. Moreover, the necessary variation for generating the H. paradoxus phenotype existed only in the BC2 population, but not in samples of the two parental species, H. annuus and H. petiolaris. These results are consistent with the hypothesis that transgressive segregation of elemental uptake and leaf succulence contributed to the origin of salt adaptation in the diploid hybrid species H. paradoxus.
Diploid hybrid speciation in plants is often accompanied by rapid ecological divergence between incipient neospecies and their parental taxa. One plausible means by which novel adaptation in hybrid lineages may arise is transgressive segregation, that is, the generation of extreme phenotypes that exceed those of the parental lines. Early generation (BC 2 ) hybrids between two wild, annual sunflowers, Helianthus annuus and Helianthus petiolaris, were used to study directional selection on transgressive characters associated with the origin of Helianthus paradoxus, a diploid hybrid species adapted to extremely saline marshes. The BC 2 plants descended from a single F 1 hybrid backcrossed toward H. petiolaris. The strength of selection on candidate adaptive traits in the interspecific BC 2 was measured in natural H. paradoxus salt marsh habitat. Positive directional selection was detected for leaf succulence and Ca uptake, two traits that are known to be important in salt stress response in plants. Strong negative directional selection operated on uptake of Na and correlated elements. A significant decrease in trait correlations over time was observed in the BC 2 population for Na and Ca content, suggesting an adaptive role for increased Ca uptake coupled with increased net exclusion of Na from leaves. Patterns of directional selection in BC 2 hybrids were concordant with character expression in the natural hybrid species, H. paradoxus, transplanted into the wild. Moreover, the necessary variation for generating the H. paradoxus phenotype existed only in the BC 2 population, but not in samples of the two parental species, H. annuus and H. petiolaris. These results are consistent with the hypothesis that transgressive segregation of elemental uptake and leaf succulence contributed to the origin of salt adaptation in the diploid hybrid species H. paradoxus.
The diploid hybrid species Helianthus paradoxus is restricted to salt marshes with sodium concentrations that exceed those found in the habitats of its progenitors, H. annuus and H. petiolaris. The observed association with saline habitats has led to the hypothesis that H. paradoxus is more salt tolerant than its progenitors. This hypothesis was tested by growing all three species in three NaCl treatments (0 mmol/L, 100 mmol/L, and 200 mmol/L). Helianthus paradoxus treated with NaCl was found to be more than five times as fit, in terms of biomass and survivorship, than its progenitors. Selection for salt tolerance in early generation hybrids may have contributed to the formation of H. paradoxus because theory predicts that homoploid hybrid speciation is feasible even when selection favoring hybrid genotypes is much weaker. Additionally, we show that H. paradoxus is significantly different from its parental species for several traits that often distinguish salt-tolerant species and suggest a mechanistic basis for the elevated salt tolerance expressed by H. paradoxus.
It is currently thought that most angiosperms transmit their mitochondrial genomes maternally. Maternal transmission limits opportunities for genetic heterogeneity (heteroplasmy) of the mitochondrial genome within individuals. Recent studies of the gynodioecious species Silene vulgaris and Silene acaulis, however, document both direct and indirect evidence of mitochondrial heteroplasmy, suggesting that the mitochondrial genome is at times transmitted via paternal leakage. This heteroplasmy allows the generation of multi-locus recombinants, as documented in recent studies of both species. A prior study that employed quantitative PCR (q-PCR) on a limited sample provided direct evidence of heteroplasmy in the mitochondrial gene atp1 in S. vulgaris. Here, we apply the q-PCR methods to a much larger sample and extend them to incorporate the study of an additional atp1 haplotype along with two other haplotypes of the mitochondrial gene cox1 to evaluate the origin, extent, and transmission of mitochondrial genome heteroplasmy in S. vulgaris. We first calibrate our q-PCR methods experimentally and then use them to quantify heteroplasmy in 408 S. vulgaris individuals sampled from 22 natural populations located in Virginia, New York, and Tennessee. Sixty-one individuals exhibit heteroplasmy, including five that exhibited the joint heteroplasmy at both loci that is a prerequisite for effective recombination. The heteroplasmic individuals were distributed among 18 of the populations studied, demonstrating that heteroplasmy is a widespread phenomenon in this species. Further, we compare mother and offspring from 71 families to determine the rate of heteroplasmy gained and lost via paternal leakage and vegetative sorting across generations. Of 17 sibships exhibiting cox1 heteroplasmy and 14 sibships exhibiting atp1 heteroplasmy, more than half of the observations of heteroplasmy are generated via paternal leakage at the time of fertilization, with the rest being inherited from a heteroplasmic mother. Moreover, we show that the average paternal contribution during paternal leakage is about 12%. These findings are surprising, given that the current understanding of gynodioecy assumes that mitochondrial cytoplasmic male sterility elements are strictly maternally inherited. Knowledge of the dynamics of mitochondrial populations within individuals plays an important role in understanding the evolution of gynodioecy, and we discuss our findings within this context.
Spread of the invasive cactus-feeding moth Cactoblastis cactorum has been well documented since its export from Argentina to Australia as a biocontrol agent, and records suggest that all non-native populations are derived from a single collection in the moth's native range. The subsequent global spread of the moth has been complex, and previous research has suggested multiple introductions into North America. There exists the possibility of additional emigrations from the native range in nursery stock during the late twentieth century. Here, we present mitochondrial gene sequence data (COI) from South America (native range) and North America (invasive range) to test the hypothesis that the rapid invasive spread in North America is enhanced by unique genetic combinations from isolated portions of the native range. We found that haplotype richness in the native range of C. cactorum is high and that there was 90% lower richness in Florida than in Argentina. All Florida C. cactorum haplotypes are represented in a single, well-defined clade, which includes collections from the reported region of original export from Argentina. Thus, our data are consistent with the documented history suggesting a single exportation of C. cactorum from the eastern region of the native range. Additionally, the presence of geographic structure in three distinct haplotypes within the same clade across Florida supports the hypothesis of multiple introductions into Florida from a location outside the native range. Because the common haplotypes in Florida are also known to occur in the neighboring Caribbean Islands, the islands are a likely source for independent North American colonization events. Our data show that rapid and successful invasion within North America cannot be attributed to unique genetic combinations. This suggests that successful invasion of the southeastern US is more likely the product of a fortuitous introduction into favorable abiotic conditions and/or defense responses of specific Opuntia hosts, rapid adaptation, or a release from native enemies.
Populations of mitochondria reside within individuals. Among angiosperms, these populations are rarely considered as genetically variable entities and typically are not found to be heteroplasmic in nature, leading to the widespread assumption that plant mitochondrial populations are homoplasmic. However, empirical studies of mitochondrial variation in angiosperms are relatively uncommon due to a paucity of sequence variation. Recent greenhouse studies of Silene vulgaris suggested that heteroplasmy might occur in this species at a level that it is biologically relevant. Here, we use established qualitative methods and a novel quantitative PCR method to study the intraindividual population genetics of mitochondria across two generations in natural populations of S. vulgaris. We show incidences of heteroplasmy for mitochondrial atpA and patterns of inheritance that are suggestive of more widespread heteroplasmy at both atpA and cox1. Further, our results demonstrate that quantitative levels of mitochondrial variation within individuals are high, constituting 26% of the total in one population. These findings are most consistent with a biparental model of mitochondrial inheritance. However, selection within individuals may be instrumental in the maintenance of variation because S. vulgaris is gynodioecious. Male sterility is, in part, regulated by the mitochondrial genome, and strong selection pressures appear to influence the frequency of females in these populations.
Chloroplast DNA (cpDNA) is maternally inherited in the majority, but not all, of angiosperm species. The mode of inheritance of cpDNA is a critical determinant of its molecular evolution and of its population genetic structure. Here, we present the results of investigations of the inheritance of cpDNA in Silene vulgaris, a plant used in a variety of studies in which cpDNA is an important component. PCR/RFLP markers were used to compare mother and offspring cpDNA genotypes sampled from two natural populations, and mother, father, and offspring genotypes obtained from controlled greenhouse crosses. Ten of 215 offspring cpDNA genotypes studied in the controlled crosses and three of 156 offspring from natural populations did not match that of the mother, demonstrating rare nonmaternal inheritance. That the chloroplast genome is occasionally transmitted through pollen is discussed in the context of using S. vulgaris cpDNA as a marker in studies of seed dispersal and when considering the joint evolution of the chloroplast and mitochondrial genomes.
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