Evolutionary genetics: jumping into a new species.
A new study finds a dramatic increase in transposable element numbers in three new sunflower hybrid species, and may suggest a novel role for transposable elements in speciation.
Genetic Speciation↗
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Interspecific hybridization increases transposition rates of Osvaldo.
Several authors have postulated that genetic divergence between populations could result in genomic incompatibilities that would cause an increase in transposition in their hybrids, producing secondary effects such as sterility and therefore starting a speciation process. It has been demonstrated that transposition largely depends on intraspecific hybridization for P, hobo, and I elements in Drosophila melanogaster and for several elements, including long terminal repeat (LTR) and non-LTR retrotransposons, in D. virilis. However, in order to demonstrate the putative effect of transposable elements on speciation, high levels of transposition should also be induced in hybrids between species that could have been originated by this process and that are still able to interbreed. To test this hypothesis, we studied the transposition of the LTR retrotransposon Osvaldo in Drosophila buzzatii-Drosophila koepferae hybrids. We used a simple and robust experimental design, analyzing large samples of single-pair mate offspring, which allowed us to detect new insertions by in situ hybridization to polytene chromosomes. In order to compare transposition rates, we also used a stock recently obtained from the field and a highly inbred D. buzzatii strain. Our results show that the transposition rate of Osvaldo is 10(-3) transpositions per element per generation in all nonhybrid samples, very high when compared with those of other transposable elements. In hybrids, the transposition rate was always 10(-2), significantly higher than in nonhybrids. We show that inbreeding has no effect on transposition in the strains used, concluding that hybridization significantly increases the Osvaldo transposition rate.
Animals↗
The tree Cedrela odorata (Meliaceae): a morphologically subdivided species in Costa Rica.
In Latin America. Cedrela odorata is a wide ranging species that occurs in several environments, where it shows significant morphological variation. A common garden experiment was established with seedlings from 63 families of ten populations from two habitat types (mesic and dry), distributed throughout Costa Rica, to examine the relationships between quantitative variation and site of population origin. Seedlings from dry areas tended to be distinct from those from mesic areas, with climatic grouping of provenance explaining a mean of 52% of the total variance and 80% of the genetic variance. Cluster analysis for seedling traits showed two natural groupings of families, which corresponded for the most part with the regional population groupings into mesic (Atlantic and South Pacific) and dry (North Pacific) groups. Cluster analysis based on seed weight and size also separated populations into mesic and dry climatic groups. Seeds from populations in dry areas were 43% heavier, and seedlings were 61% taller, 117% greater in diameter, and with leaflets 39% longer and 81% wider. These differences may be related to fast growth in the dry zone for taking advantage of early life cycle moisture availability. These findings may indicate incipient speciation in C. odorata in Costa Rica. Evaluation of reproductive isolating mechanisms between populations from the mesic and dry zones, and of clines at potential zones of hybridization would assist in testing a speciation hypothesis.
Analysis of Variance↗
A comparison of multilocus clines maintained by environmental adaptation or by selection against hybrids.
There has recently been considerable debate over the relative importance of selection against hybrids ("endogenous" selection) vs. adaptation to different environments ("exogenous") in maintaining stable hybrid zones and hence in speciation. Single-locus models of endogenous and exogenous viability selection generate clines of similar shape, but the comparison has not been extended to multilocus systems, which are both quantitatively and qualitatively very different from the single-locus case. Here we develop an analytical multilocus model of differential adaptation across an environmental transition and compare it to previous heterozygote disadvantage models. We show that the shape of clines generated by exogenous selection is indistinguishable from that generated by endogenous selection. A stochastic simulation model is used to test the robustness of the analytical description to the effects of drift and strong selection, and confirms the prediction that pairwise linkage disequilibria are predominantly generated by migration. However, although analytical predictions for the width of clines maintained by heterozygote disadvantage fit well with the simulation results, those for environmental adaptation are consistently too narrow; reasons for the discrepancy are discussed. There is a smooth transition between a system in which a set of loci effectively act independently of each other and one in which they act as a single nonrecombining unit.
Adaptation, Physiological↗
Rapid genomic changes in interspecific and intergeneric hybrids and allopolyploids of Triticeae.
Allopolyploidy is preponderant in plants, which often leads to speciation. Some recent studies indicate that the process of wide hybridization and (or) genome doubling may induce rapid and extensive genetic and epigenetic changes in some plant species and genomic stasis in others. To further study this phenomenon, we analyzed three sets of synthetic allopolyploids in the Triticeae by restriction fragment length polymorphism (RFLP) using a set of expressed sequence tags (ESTs) and retrotransposons as probes. It was found that 40-64.7% of the ESTs detected genomic changes in the three sets of allopolyploids. Changes included disappearance of parental hybridization fragment(s), simultaneous appearance of novel fragment(s) and loss of parental fragment(s), and appearance of novel fragment(s). Some of the changes occurred as early as in the F1 hybrid, whereas others occurred only after allopolyploid formation. Probing with retrotransposons revealed numerous examples of disappearance of sequences. No gross chromosome structural changes or physical elimination of sequences were found. It is suggested that DNA methylation and localized recombination at the DNA level were probably the main causes for the genomic changes. Possible implications of the genomic changes for allopolyploid genome evolution are discussed.
Cytosine↗
Speciation and inversions: chimps and humans.
A new set of models has resurrected a role for chromosomal inversions in the formation of new species. Traditional models, which are generally considered to be unlikely in most cases, had imagined that inversions might aid speciation by directly causing low hybrid fitness. In contrast, the newer models focus on the effect that inversions have on local recombination rates. A test of these models found a strikingly high rate of amino-acid substitution within regions where humans and chimpanzees differ by inversions, suggesting perhaps that our ancestral species underwent a divergence process in which gene flow and inversions played a key role. However, it remains uncertain whether this interesting finding is actually consistent with the proposed model.
Animals↗
Incomplete cryptic speciation between intertidal and subtidal morphs of Acrocnida brachiata (Echinodermata: Ophiuroidea) in the Northeast Atlantic.
The brittle-star Acrocnida brachiata (Montagu) lives in sandy-bottom habitat of both intertidal and subtidal zones along the coasts of the northwestern Europe. An allozyme frequency-based survey (five enzyme loci) was combined with a mitochondrial (mt) COI haplotype analysis (598-bp sequences) on 17 populations to trace back past colonization pathways from the actual population structure of the species. Both genetic markers display a sharp genetic break between intertidal (clade I) and subtidal populations (clade S). This break corresponds to an allele frequency inversion at three enzyme loci (Hk, Pgm and Pgi) and a deep divergence of about 20% in mtCOI sequences between most of the intertidal populations and other samples. The geographic distribution of clade I seems to be more restricted than clade S as it is absent from the intertidal of the eastern English Channel and North Sea and may be replaced by clade S in south Brittany. Applying previously published rates of mutation, divergence between the two clades is estimated to pre-date 5 million years ago and may be due to allopatric speciation processes at the Mio-Pliocene transition. The occurrence of putative hybrids in a few localities, however, suggests incomplete cryptic speciation with secondary contact zones. The relative importance of colonization history vs. habitat specialization are discussed in the light of neutral evolution as tested from mtCOI gene sequences. While differential selection seems to have contributed little to the separation of the lineages, it may have played a role in the emergence of adaptive polymorphisms in the hybrid zone. Furthermore, congruent spatial patterns of differentiation were observed in both clades suggesting a recent increase in population size. These findings are in agreement with a recent expansion of the populations during or after the formation of the English Channel, from a southern refuge for the subtidal clade whereas the intertidal clade may have persisted further north. As previously suspected for a species with a very short pelagic larval phase, contemporary gene flow between distant or adjacent populations appears to be extremely reduced or even absent.
Animals↗
Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella.
In On the Origin of Species, Darwin proposed that natural selection had a fundamental role in speciation. But this view receded during the Modern Synthesis when allopatric (geographic) models of speciation were integrated with genetic studies of hybrid sterility and inviability. The sympatric hypothesis posits that ecological specialization after a host shift can result in speciation in the absence of complete geographic isolation. The apple maggot, Rhagoletis pomonella, is a model for sympatric speciation in progress. Hawthorn (Crataegus spp.) is the native host for R. pomonella in N. Americas. But in the mid-1800s, a new population formed on introduced, domesticated apple (Malus pumila). Recent studies have conferred 'host race' status on apple flies as a potentially incipient species, partially isolated from haw flies owing to host-related adaptation. However, the source of selection that differentiates apple and haw flies is unresolved. Here we document a gene-environment interaction (fitness trade-off) that is related to host phenology and that genetically differentiates the races.
Animals↗
Divergent genetic and epigenetic post-zygotic isolation mechanisms in Mus and Peromyscus.
Interspecific hybridization in the rodent genera Peromyscus and Mus results in abnormal placentation. In the Peromyscus interspecies hybrids, abnormal allelic interaction between an X-linked locus and the imprinted paternally expressed Peg3 locus was shown to cause the placental defects. In addition, loss-of-imprinting (LOI) of Peg3 was positively correlated with increased placental size. As in extreme cases this placental dysplasia constitutes a post-zygotic barrier against interspecies hybridization, this finding was the first direct proof that imprinted genes may be important in speciation and thus in evolution. In the Mus interspecies hybrids, a strong role of an X-linked locus in placental dysplasia has also been detected. However, here we show by backcross and allele specific expression analyses that neither LOI of Peg3 nor abnormal interactions between Peg3 and an X-linked locus are involved in generating placental dysplasia in Mus hybrids, although the placental phenotypes observed in the two genera seem to be identical. In contrast to this, another dysgenesis effect common to Peromyscus and Mus hybrids, altered foetal growth, is caused at least in part by the same X-chromosomal regions in both genera. These findings first underline the strong involvement of the X-chromosome in the genetics of speciation. Secondly, they indicate that disruption of epigenetic states, such as LOI, at specific loci may be involved in hybrid dysgenesis effects in one group, but not in another. Thus, we conclude that even in closely related groups divergent molecular mechanisms may be involved in the production of phenotypically similar post-zygotic barriers against hybridization.
Alleles↗
The genetic architecture of male colour differences between a sympatric Lake Malawi cichlid species pair.
The genetic basis of traits involved in reproductive isolation is a key parameter in models of sympatric speciation by sexual selection, a potential mechanism driving the explosive radiation of East African cichlids. Analysis of hybrid crosses between two sympatric Lake Malawi cichlid species, representing the extremes of the extant colour distribution, generated Castle-Wright estimates of four to seven loci controlling colour differences. Segregation patterns deviated from a purely additive model with a significant contribution from dominance, and possibly also epistasis. Evidence was found for a strong influence of autosomal loci. As departures from simple additive variation could effect the operation of models of sympatric speciation, dominance and epistasis should not be neglected.
Animals↗
Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation.
It is generally believed that Drosophila melanogaster has no closely related species with which it can produce the viable and fertile hybrids that are essential for the genetic analysis of speciation. Following the recent report of molecular differentiation between a Zimbabwe, Africa, population and two United States populations, we provide evidence that strong sexual isolation exists between the D. melanogaster population in Zimbabwe and populations of other continents. In the presence of males of their own kind, females from most isofemale lines of Zimbabwe would not mate with males from elsewhere; the reciprocal mating is also significantly reduced, but to a lesser degree. The genes for sexual behaviors are apparently polymorphic in Zimbabwe and postmating reproductive isolation between this and other populations has not yet evolved. Whole chromosome substitutions indicate significant genetic contributions to male mating success by both major autosomes, whereas the X chromosome effect is too weak to measure. In addition, the relative mating success between hybrid and pure line males supports the interpretation of strong female choice. These observations suggest that we are seeing the early stages of speciation in this group and that it is driven by sexual selection. The genetic and molecular tractability of D. melanogaster offers great promise for the detailed analysis of this apparent case of incipient speciation.
Animals↗
Reconstructing the origin of Helianthus deserticola: survival and selection on the desert floor.
The diploid hybrid species Helianthus deserticola inhabits the desert floor, an extreme environment relative to its parental species Helianthus annuus and Helianthus petiolaris. Adaptation to the desert floor may have occurred via selection acting on transgressive, or extreme, traits in early hybrids between the parental species. We explored this possibility through a field experiment in the hybrid species' native habitat using H. deserticola, H. annuus, H. petiolaris, and two populations of early-generation (BC(2)) hybrids between the parental species, which served as proxies for the ancestral genotype of the ancient hybrid species. Character expression was evaluated for each genotypic class. Helianthus deserticola was negatively transgressive for stem diameter, leaf area, and flowering date, and the latter two traits are likely to be advantageous in a desert environment. The BC(2) hybrids contained a range of variation that overlapped these transgressive trait means, and an analysis of phenotypic selection revealed that some of the selective pressures on leaf size and flowering date, but not stem diameter, would move the BC(2) population toward the H. deserticola phenotype. Thus, H. deserticola may have originated from habitat-mediated directional selection acting on hybrids between H. annuus and H. petiolaris in a desert environment.
Adaptation, Physiological↗
Evolutionary paths underlying flower color variation in Antirrhinum.
To understand evolutionary paths connecting diverse biological forms, we defined a three-dimensional genotypic space separating two flower color morphs of Antirrhinum. A hybrid zone between morphs showed a steep cline specifically at genes controlling flower color differences, indicating that these loci are under selection. Antirrhinum species with diverse floral phenotypes formed a U-shaped cloud within the genotypic space. We propose that this cloud defines an evolutionary path that allows flower color to evolve while circumventing less-adaptive regions. Hybridization between morphs located in different arms of the U-shaped path yields low-fitness genotypes, accounting for the observed steep clines at hybrid zones.
Adaptation, Biological↗
The evolution of California's wild radish has resulted in the extinction of its progenitors.
If two previously isolated taxa mutually assimilate through hybridization and subsequent biparental introgression, and if their introgressed descendants have the same or higher fitness than their parents, then gene flow should result in the local extinction of parental taxa via replacement by hybrid derivatives. These dramatic events may occur rapidly, even in a few generations. Given the speed at which such extinction by hybridization may occur, it may be difficult to identify that the process has occurred. Thus, documented instances of extinction by hybridization are rare, and especially so for cases in which both parents are replaced by the hybrid lineage. Here we report morphological and allozyme evidence for the local extinction of two Raphanus species in California via replacement by their hybrid-derived descendants. The results from a greenhouse experiment demonstrate that California wild radishes have a specific combination of traits from their progenitors, and comparison of our results to that of an earlier report indicate that pure parental types are no longer present in the wild. Our results also show the hybrid-derived lineage has transgressive fruit weight compared to its parents. Allozyme analysis demonstrates that California wild radishes are derived from hybridization between the putative parental species. However, that analysis also demonstrates that California wild radish has now become an evolutionary entity separate from both of its parents. We suggest that the aggressive colonizing behavior of the hybrid-derived lineage probably results from a novel combination of parental traits, rather than genetic variability of the population per se.
Biodiversity↗
Evolution of sexual isolation in laboratory populations: fitness differences between mating types and the associated hybrid incompatibilities.
Drosophila melanogaster is known to have two races in the incipient stages of speciation that exhibit strong asymmetric premating isolation: Zimbabwe (Z) and cosmopolitan (M). In a study examining the phenotypic and genotypic evolution after secondary contact, we found that despite strong sexual selection favoring the Z-type behavior, it is the M-type behavior that comes to dominate hybrid populations. This article examines the fitness costs associated with the Z-type behavior. We have discovered that these costs are great enough to explain the failure of the Z-type behavior to prosper. Here we report that Z-type females produce approximately half the number of offspring that M-type females produce. Furthermore, crosses between populations have revealed that Z-type females mated to M-type males have approximately 20% fewer offspring than the reciprocal crosses because of an inability of M-type sperm to successfully fertilize Z-type eggs. Hybrid crosses also exhibit much-reduced numbers of viable offspring in addition to reduced hybrid male fertility. These fitness effects suggest that multiple mechanisms of postmating isolation have evolved concurrently with the divergence in behavior.
Animals↗
Reinforcement and the genetics of hybrid incompatibilities.
Recent empirical studies suggest that genes involved in speciation are often sex-linked. We derive a general analytic model of reinforcement to study the effects of sex linkage on reinforcement under three forms of selection against hybrids: one-locus, two-locus, and ecological incompatibilities. We show that the pattern of sex linkage can have a large effect on the amount of reinforcement due to hybrid incompatibility. Sex linkage of genes involved in postzygotic isolation generally increases the strength of reinforcement, but only if genes involved in prezygotic isolation are also sex linked. We use exact simulations to test the accuracy of the approximation and find that qualitative predictions made assuming weak selection can hold when selection is strong. Our simulations also show that incompatibilities that evolve in allopatry by drift or weak selection are likely to be lost by swamping during secondary contact, even when selection against hybrids is strong.
Alleles↗
Hybridization and reproductive isolation among syntopic populations of the topminnows Fundulus notatus and F. olivaceus.
Fundulus notatus and Fundulus olivaceus are two closely related topminnow species that exhibit similar ecological niches and broad, largely overlapping, North American ranges extending throughout much of the Mississippi River drainage as well as the coastal drainages of the Gulf of Mexico. Previous studies have suggested that these two species are reproductively compatible despite cytogenetic differences and will hybridize when syntopic. We used nuclear and mtDNA loci to assess levels of hybridization and test for introgression in syntopic populations of these two species in four drainages in southern Illinois. Although hybridization was detected in all syntopic populations, an assessment of the proportion of hybrid individuals indicated a deficiency of hybrids relative to expectations under random mating. We determined that, although mtDNA introgression was prevalent and extended beyond the zones of contact, evidence of nuclear introgression was limited to the zone of sympatry.
Animals↗
The basis of natural and artificial postzygotic hybridization barriers in Arabidopsis species.
The success or failure of interspecific crosses is vital to evolution and to agriculture, but much remains to be learned about the nature of hybridization barriers. Several mechanisms have been proposed to explain postzygotic barriers, including negative interactions between diverged sequences, global genome rearrangements, and widespread epigenetic reprogramming. Another explanation is imbalance of paternally and maternally imprinted genes in the endosperm. Interspecific crosses between diploid Arabidopsis thaliana as the seed parent and tetraploid Arabidopsis arenosa as the pollen parent produced seeds that aborted with the same paternal excess endosperm phenotype seen in crosses between diploid and hexaploid A. thaliana. Doubling maternal ploidy restored seed viability and normal endosperm morphology. However, substituting a hypomethylated tetraploid A. thaliana seed parent reestablished the hybridization barrier by causing seed abortion and a lethal paternal excess phenotype. We conclude from these findings that the dominant cause of seed abortion in the diploid A. thaliana x tetraploid A. arenosa cross is parental genomic imbalance. Our results also demonstrate that manipulation of DNA methylation can be sufficient to erect hybridization barriers, offering a potential mechanism for speciation and a means of controlling gene flow between species.
Arabidopsis↗