How can very small differences in nucleotide sequences

As a general consequence, this finding would implicate genetic drift as a very strong, long-term evolutionary force in highly social honeybees. The even lower divergence and overall coalescence times of A. This is seen by the significantly shorter internal branches when compared with other branches of the phylogeny fig.

Such a burst of diversification after a population bottleneck has been previously described for self-incompatibility alleles of Physalis crassifolia Richman et al. We hypothesize that small long-term population size in these honeybees is a consequence of highly social organization. The strong division of reproduction among individuals under highly social organization results in a dramatic decrease in long-term effective population size Wilson ; Crozier ; Pamilo and Crozier Thousands of sterile female worker bees are headed by a single reproductive queen, thus substantially reducing the size of the breeding population relative to the total number of individuals that can be sustained by the local environment.

Under balancing selection, the estimate of N e is not strongly affected by population structure Schierup et al. The long-term estimates can be related to short-term estimates of effective population size based on neutral polymorphism data for A.

This is supported by biogeographic molecular studies that have shown an expansion and differentiation of A. In contrast to strongly balanced polymorphisms, these neutral polymorphisms are strongly affected by the substructure of populations thus making both estimates less comparable.

We identified a substantial excess of shared nonsynonymous changes at csd -PSD that accumulated independently in different alleles across species homoplasy. This provides indirect evidence that positive selection has favored some specific nonsynonymous changes.

The lack of trans-specific alleles and the absence of an excess of synonymous changes suggest that the excess of shared nonsynonymous changes have an independent evolutionary origin. Our approximation is constant over all species pairs, suggesting that equivalent evolutionary constraints at csd -PSD are operating across species.

The polymorphisms that evolved convergently at csd -PSD could be very informative to identify molecular determinants of allelic specificity. Significantly, these shared sites are scattered across csd -PSD, suggesting that functionally relevant polymorphisms are not confined to a specific region. The hypervariable region most likely adds to the specificity of alleles. We identified 2 basic peptide motifs across species, suggesting their evolutionary origin in a common ancestor.

These regions further diversify in the different honeybee lineages essentially by changing the number of repeats. A recent study Cho et al. Our study, which includes a sophisticated set of alleles relying on transcribed sequences thus excluding possible noncoding sequences of the genomic fragment approach [ Cho et al. Balancing selection has enhanced the relative rate of accumulation of nonsynonymous changes among newly diverged alleles. These enhanced evolutionary rates of newly diverged alleles may also explain our previous report on longer terminal over internal branches in the csd genealogy Hasselmann and Beye This longer terminal branch pattern is unexpected from theory Uyenoyama but has also been reported for S allele genealogies Richman and Kohn Overall, this study has deciphered a complex pattern of evolutionary forces selection, genetic drift, mutation, and recombination that have shaped nucleotide polymorphism at csd -PSD and linked sites.

A conclusive test of these evolutionary genetic evidences awaits detailed functional analysis. This will provide further evidence that the csd -PSD corresponds to the specifying domain and that shared polymorphisms are informative to identify the molecular determinants of allele specificity and protein activation Beye et al. This merged approach will give a more detailed understanding of how selection has shaped nucleotide diversity and the function of alleles.

Extending studies on allelic richness and nucleotide diversity to other bee species will decipher whether social organization is generally associated with a high turnover rate of sex determination alleles and small long-term effective population sizes.

Such a general association will have implications for the understand of natural selection in relation to social organization Pamilo and Crozier and may have broad consequences such as genome-wide high recombination rates Beye et al.

We thank very much Ross Crozier, George Heimpel, Robert Paxton, and 2 anonymous reviewers for very helpful comments and corrections on an earlier version of the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft.

Google Scholar. Google Preview. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign In. Advanced Search. Search Menu. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents Abstract.

Materials and Methods. Martin Hasselmann , Martin Hasselmann. Oxford Academic. Xavier Vekemans. Jochen Pflugfelder.

Nikolaus Koeniger. Gudrun Koeniger. Salim Tingek. Martin Beye. Diethard Tautz, Associate Editor. Select Format Select format.

Permissions Icon Permissions. Abstract Our understanding of the impact of recombination, mutation, genetic drift, and selection on the evolution of a single gene is still limited. The derivation assumes that new functional alleles are continuously generated under an infinite-allele model of mutation. It also assumes a finite population of N f and N m reproductive females and males, respectively, where females are always heterozygotes at csd and males are strictly haploids.

Using diffusion approximations, Yokoyama and Nei showed that the homozygosity F at the sex-determining locus is given by. Finally, the pairwise coalescence time of alleles T d at csd is given by Takahata Open in new tab Download slide.

S N Apis mellifera Sample size i 15 Mean 3. Open in new tab. Estimation of the number of sex alleles and queen matings from diploid male frequencies in a population of Apis mellifera. Google Scholar PubMed. Phylogenetic relationships of honey bees Hymenoptera:Apinae:Apini inferred from nuclear and mitochondrial DNA sequence data.

Google Scholar Crossref. Search ADS. The dice of fate: the csd gene and how its allelic composition regulates sexual development in the honey bee, Apis mellifera. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Plant self-incompatibility in natural populations: a critical assessment of recent theoretical and empirical advances. Haplotype structure of the stigmatic self-incompatibility gene in natural populations of Arabidopsis lyrata.

Evolution of the complementary sex-determination gene of honey bees: balancing selection and trans-species polymorphisms. Quantifying the slightly deleterious mutation model of molecular evolution.

Evolutionary history of the honeybee Apis mellifera inferred from mitochondrial DNA analysis. Pronounced differences of recombination activity at the sex determination locus SDL of the honey bee, a locus under strong balancing selection.

Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment.

Self-incompatibility alleles from Physalis: implications for historical inference from balanced genetic polymorphisms. Allelic diversity and gene genealogy at the self-incompatibility locus in the Solanaceae. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. The effect of subdivision on variation at multi-allelic loci under balancing selection.

A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Mechanisms of molecular evolution: introduction to molecular paleopopulation biology. Polymorphism and balancing selection at major histocompatibility complex loci. A generalized least-squares estimate for the origin of sporophytic self-incompatibility. Genealogical structure among alleles regulating self-incompatibility in natural populations of flowering plants. Eye colour, skin tone and face shape are all determined by our genes so any variation that occurs will be due to the genes inherited from our parents.

In contrast, although weight is partly influenced by our genetics , it is strongly influenced by our environment. For example, how much we eat and how often we exercise. Genetic variation can also explain some differences in disease susceptibility and how people react to drugs. Genetic variation is important in evolution. Evolution relies on genetic variation that is passed down from one generation to the next.

This is known as natural selection. Related Content:. What is DNA? What is a gene? What is inheritance? What is evolution? What is a genetic disorder? What is a mutation? Because knockout lines of genes for nicotinamide adenine dinucleotide phosphate dehydrogenase NDH subunits in tobacco display no or only subtle phenotypes Burrows et al.

The differences located in promoter sequences of the Oenothera plastomes were compared with the genetically determined compatibility relationships in interspecific hybrids fig. The polymerases recognize distinct sites in plastid promoters. In all, 38 putative PEP- and 25 NEP-binding sites that were computationally predicted were altered in at least one of the plastomes Greiner et al. Mutations were classified according to 3 criteria: 1 their similarity to an ideal consensus Silhavy and Maliga ; Kapoor and Sugiura ; Homann and Link ; Kanamaru and Tanaka ; Shiina et al.

Three promoter sequences indicated drastic changes for both polymerases: the promoter of trn G GCC harboring mutations specific for plastome V, and the bidirectional promoters for clp P encoding a catalytic subunit of the protease Clp and psb B encoding the chlorophyll a —binding protein CP47 of the PSII core complex that contain a large deletion specific for plastome I.

This approach finally correlated the AB-I phenotype with a single major locus, the intergenic region psb B— clp P. AB-I displays a yellow—green lutescent phenotype fig. In this distinct case, changes in plastome I shared with or similar to at least one in plastomes II—IV can be disregarded.

They are fully bleached, largely pollen sterile, and display severe inhibition of cell division Stubbe The principal genetic determinants responsible for their phenotypes are presumably complex and different from those causing bleaching of AB-I individuals see Discussion. The outlined filtering strategy uncovered 22 regions, including minor changes such as single nucleic acid exchanges in noncoding regions. Six of them are polymorphic within all plastomes.

Sixteen regions specifically altered in plastome I remain. They are not of functional relevance because the translational apparatus is not notably affected in AB-I as could be judged by silver staining of thylakoid membrane proteins fig.

Therefore, only 2 regions remain, which serve as putative candidates. The involvement of the psb I promoter in the AB-I phenotype is rather unlike because 1 mRNA levels of psb I are not changed data not shown and 2 a knockout of psb I shows no apparent phenotype Schwenkert et al.

Consequently, only the bp deletion at position 77, of plastome I joh GenBank accession number AJ Three approaches were employed to substantiate this deduction. Positions of the indicated transcription start sites black arrows of NEP and PEP promoters P clp P and P psb B relative to the start codons were determined experimentally in Arabidopsis , tobacco, and spinach Westhoff ; Hajdukiewicz et al. Putative, not experimental verified promoters in Oenothera are marked with filled triangles. The experimentally verified P clp P and P psb B are highly conserved and confirmed bioinformatically in Oenothera and all references species.

The deletion open triangle is not present in Oenothera plastomes II—V or plastomes of other species sequenced so far and, therefore, specific for plastome I in Oenothera.

First, sequence analysis of intraplastome variance Herrmann et al. Furthermore, all these subplastomes were checked genetically, and only plastome I variants were found to cause incompatibility with genotype AB see references in supplementary table 1 , Supplementary Material online. Second, a phylogenetic footprinting analysis of the intergenic region between both genes delimited distinct boxes in the promoter region described for clp P Sriraman et al.

NPQ increased dramatically from 0. Studies on photosystem II yield and redox kinetics of photosystem I. Fluorescence induction traces induced by saturating white-light pulses showed the maximal fluorescence raise during the light pulse Fm. The Fm levels were normalized to equal heights. Dark-adapted leaves were exposed to consecutive saturating light pulses during application of continuous actinic light.

Subsequent saturating light pulses squiggled arrows on the FR background light transiently reduced PSI completely in compatible but only partially in incompatible leaves again indicating a limitation of PSII activity.

The extent of PSI oxidation in terms of balanced electron flow from PSII to PSI was monitored using absorption changes at nm on actinic background light in order to further substantiate the primary lesion in the hybrid fig.

A detailed molecular analysis of the incompatible AB-1 phenotype will be presented in a forthcoming study. Compartmental coevolution is accompanied by distinct changes in the 5 available Onagracean organelle chromosomes and the respective nuclear genomes.

In subsection Oenothera , relationships between plastome and genome are crucial for the vitality of interspecific hybrids Stubbe ; Dietrich et al. All its species can be crossed with one another, forming seeds with fully developed hybrid embryos that usually germinate and produce fertile progeny. However, the development of such hybrids is frequently disturbed and limited only by incompatibilities between the plastome of one parent plant with the genotype of the other one when the genetic compartments were not coevolved fig.

Reversibility of interspecific compartmental incompatibility is a distinguishing feature to nuclear and plastid mutations affecting the organelle; an incompatible plastid foreign to a nucleus, for instance, will regreen if recombined with its genuine genome.

Therefore, PGI is not based on mutations in single genes but in changed interactions of coevolved gene pairs, one of which resides in the chloroplast, the other in the nuclear genome. These PGI gene pairs represent a special case of the Dobzhansky—Muller model underlying their impact in speciation processes Dobzhansky Disturbances caused by interspecific organelle exchanges normally affect a multitude of ontogenetic processes.

Both, photosynthetic performance and hybrid fertility are complex characters with a large number of potential states. Thus, PGI phenotypes are probably caused by processes that operate at many scales. Complexity also becomes apparent in various extremely disharmonic plastome—genome incompatible hybrids such as AA-V, AB-V, and BB-V, in which fertility and morphogenesis are severely affected Stubbe ; Stubbe et al.

In these cases, incompatibility may be caused by multiple Dobzhansky—Muller plastid—nuclear gene pairs. The profound knowledge of the photosynthetic process and of the biogenesis, maintenance, and adaptation of its underlying structures Herrmann and Westhoff can advantageously be used for evaluating phylogenetic questions and provide general and causal access to evolutionary relationships and speciation processes.

However, our knowledge to computationally predictable functional elements from primary sequences is limited, and Oenothera genome sequences—the complementary part on which prespeciation and coevolution processes are acting—are missing. Nevertheless, the alignment of sequence differences between plastomes of closely related, interbreeding species to predict genetic elements combined with filtering by their evolutionary and functional relevance as well as combinatorial logics is a promising strategy to pinpoint potential plastid-localized determinants involved in compartmental coevolution last not least because predictions can be tested.

The case study of the hybrid AB-I has proven that the strategy of systematic filtering on genetically well-defined material is useful and attests to the power of the method. This mutant also displays comparable fluorescence characteristics.

Loci such as the clp P— psb B intergenic region deduced by this approach are therefore potential candidates that deserve further study of underlying molecular mechanisms of PGI. At a molecular scale, coevolution of polypeptides with their interaction partners, polypeptides with polypeptides or polypeptides with nucleic acid molecules, is a well-known phenomenon Goh et al. Diverging loci supplementary table 5 , Supplementary Material online are therefore of intrinsic interest but the vast majority of such loci found in Oenothera either does not seem to be involved in interspecific compartmental incompatibility or does not contribute in a simple way.

All changes occurred in parts of polypeptide chains, which are generally highly variable and do not affect conserved domains supplementary figs. S1—S5 [Supplementary Material online] in Greiner et al. In terms of single amino acid exchanges of all detected nonsynonymous substitutions, only 35 sites from which 25 are located in functional domains show biochemically significant different properties with respect to reference plastomes supplementary table 3 , Supplementary Material online.

Current knowledge decreases this small number of candidates even further. Furthermore, a biochemically possibly significant amino acid change in pet D fits with the compatibility chart in principle fig. Collectively, the available data strongly suggest that plastome-encoded genes for structural components of the photosynthetic machinery are usually highly conserved. Species-specific editotype differences in plastid DNA and coevolving nuclear encoded trans factors have been shown to be important in compartmental coevolution between Atropa and tobacco.

They play a crucial role in harmonious nucleo—plastid interaction between both species and also explain the pronounced phenotypic difference of their reciprocal cybrids Schmitz-Linneweber et al. RNA editing obviously does not influence compartmental coevolution in evening primroses. Collectively, these findings suggest that despite of photosynthetic defects in both, Solanaceae and Oenothera , the determinants and mechanisms causing plastid—nuclear incompatability are quite different.

Obviously, the ways in which individual species or genera have evolved, their histories, and adaptation to their present-day habitats are diverse and include changes at quite different molecular levels. Plastid chromosomes have well-defined structures, a limited coding potential and a conserved design.

Their sequences have become a powerful research tool not only to probe into chloroplast biogenesis, function, and engineering but also into eukaryotic genome evolution.

Classical data sets such as available for subsection Oenothera are of obvious value to study microevolutionary processes. The other subsections of the genus have not yet received a comparably intense genetic study, but quite substantial information is available regarding interfertility and plastid—nuclear compatibility relationships Stubbe and Raven As in subsection Oenothera , offspring of interspecific crosses within subsections Raimannia , Munzia , Nutantigemma , and Emersonia is generally fertile, and even the generation of intersubsectional hybrids is possible, but these are often extremely disharmonic and their fertility is usually reduced Stubbe and Raven We thank Martina Silber for critical comments, Dario Leister for kindly reading the manuscript, and the Springer-Verlag for permission to adapt figure 2.

We dedicate this manuscript to the memory of Prof. Dr Rainer M. Google Scholar. Google Preview. Oxford University Press is a department of the University of Oxford.

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