Margarita Beltran - Academia.edu (original) (raw)

Papers by Margarita Beltran

BMC Biology, Apr 21, 2006

Background: The view that gene flow between related animal species is rare and evolutionarily uni... more Background: The view that gene flow between related animal species is rare and evolutionarily unimportant largely antedates sensitive molecular techniques. Here we use DNA sequencing to investigate a pair of morphologically and ecologically divergent, non-sibling butterfly species, Heliconius cydno and H. melpomene (Lepidoptera: Nymphalidae), whose distributions overlap in Central and Northwestern South America. Results: In these taxa, we sequenced 30-45 haplotypes per locus of a mitochondrial region containing the genes for cytochrome oxidase subunits I and II (CoI/CoII), and intron-spanning fragments of three unlinked nuclear loci: triose-phosphate isomerase (Tpi), mannose-6-phosphate isomerase (Mpi) and cubitus interruptus (Ci) genes. A fifth gene, dopa decarboxylase (Ddc) produced sequence data likely to be from different duplicate loci in some of the taxa, and so was excluded. Mitochondrial and Tpi genealogies are consistent with reciprocal monophyly, whereas sympatric populations of the species in Panama share identical or similar Mpi and Ci haplotypes, giving rise to genealogical polyphyly at the species level despite evidence for rapid sequence divergence at these genes between geographic races of H. melpomene. Conclusion: Recent transfer of Mpi haplotypes between species is strongly supported, but there is no evidence for introgression at the other three loci. Our results demonstrate that the boundaries between animal species can remain selectively porous to gene flow long after speciation, and that introgression, even between non-sibling species, can be an important factor in animal evolution. Interspecific gene flow is demonstrated here for the first time in Heliconius and may provide a route for the transfer of switch-gene adaptations for Müllerian mimicry. The results also forcefully demonstrate how reliance on a single locus may give an erroneous picture of the overall genealogical history of speciation and gene flow.

pollen feeding and pupal-mating have a single origin in Heliconius

Science, 1999

In their report “Conservatism of ecological niches in evolutionary time” (20 Aug., p. [1265][1]),... more In their report “Conservatism of ecological niches in evolutionary time” (20 Aug., p. [1265][1]), A. T. Peterson et al. demonstrate that geographically isolated sister taxa show little differentiation in ecological niche. Their results imply that ecology diverges slowly in allopatry (the geographic isolation of species), and the authors therefore conclude that speciation most commonly occurs without significant ecological change. However, this conclusion seems to contradict the observation that sympatric sister taxa (species living in the same or overlapping locations) generally do show divergent ecology. Indeed, many sympatric ecological races are so closely related that hybridization still occurs regularly ([1][2]). We suggest two possible explanations for this discrepancy. First, as mentioned in the News of the Week article by Bernice Wuethrich (20 Aug., p. [1190][3]), the analysis considered only four physical factors in defining the niche of each species. Certainly, biotic factors such as feeding strategy, host plant use (in the case of butterflies), mutualisms, and predation are also important in defining the niche of a species. Thus, it may be that the analysis was simply too crude to show ecological divergence over a relatively short time scale. Alternatively, if Peterson et al. are correct and ecological divergence does in fact proceed rather slowly in allopatry, then we need another explanation for the frequent occurrence of sympatric, ecologically divergent sister taxa. Sympatric speciation, when it occurs, is likely to proceed rapidly because disruptive selection plays a direct role in driving divergence ([2][4]). In contrast, models of allopatric speciation do not generally invoke a direct role for natural selection and might thus be expected to proceed more slowly. By showing that allopatric divergence does not lead to rapid ecological change, Peterson et al. may have provided some of the best evidence that sympatric sister species have evolved in situ. 1. [↵][5]1. M. R. Orr, 2. T. B. Smith , Trends Ecol. Evol. 13, 502 (1998). [OpenUrl][6][CrossRef][7][PubMed][8][Web of Science][9] 2. [↵][10]1. U. Dieckmann, 2. M. Doebeli , Nature 400, 354 (1999). [OpenUrl][11][CrossRef][12][GeoRef][13] [1]: /lookup/doi/10.1126/science.285.5431.1265 [2]: #ref-1 [3]: /lookup/doi/10.1126/science.285.5431.1190a [4]: #ref-2 [5]: #xref-ref-1-1 "View reference 1 in text" [6]: {openurl}?query=rft.jtitle%253DTrends%2Bin%2BEcology%2B%2526%2BEvolution%26rft.stitle%253DTrends%2Bin%2BEcology%2B%2526%2BEvolution%26rft.aulast%253DOrr%26rft.auinit1%253DM.%2BR.%26rft.volume%253D13%26rft.issue%253D12%26rft.spage%253D502%26rft.epage%253D506%26rft.atitle%253DEcology%2Band%2Bspeciation.%26rft_id%253Dinfo%253Adoi%252F10.1016%252FS0169-5347%252898%252901511-0%26rft_id%253Dinfo%253Apmid%252F21238408%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [7]: /lookup/external-ref?access_num=10.1016/S0169-5347(98)01511-0&link_type=DOI [8]: /lookup/external-ref?access_num=21238408&link_type=MED&atom=%2Fsci%2F286%2F5438%2F239.5.atom [9]: /lookup/external-ref?access_num=000077403800010&link_type=ISI [10]: #xref-ref-2-1 "View reference 2 in text" [11]: {openurl}?query=rft.jtitle%253DNature%253B%2BPhysical%2BScience%2B%2528London%2529%26rft.stitle%253DNature%253B%2BPhysical%2BScience%2B%2528London%2529%26rft.volume%253D400%26rft.issue%253D6742%26rft.spage%253D354%26rft.epage%253D357%26rft.atitle%253DOn%2Bthe%2Borigin%2Bof%2Bspecies%2Bby%2Bsympatric%2Bspeciation%26rft_id%253Dinfo%253Adoi%252F10.1038%252F22521%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [12]: /lookup/external-ref?access_num=10.1038/22521&link_type=DOI [13]: /lookup/external-ref?access_num=1999055575&link_type=GEOREF

BMC biology, Jan 21, 2006

The view that gene flow between related animal species is rare and evolutionarily unimportant lar... more The view that gene flow between related animal species is rare and evolutionarily unimportant largely antedates sensitive molecular techniques. Here we use DNA sequencing to investigate a pair of morphologically and ecologically divergent, non-sibling butterfly species, Heliconius cydno and H. melpomene (Lepidoptera: Nymphalidae), whose distributions overlap in Central and Northwestern South America. In these taxa, we sequenced 30-45 haplotypes per locus of a mitochondrial region containing the genes for cytochrome oxidase subunits I and II (CoI/CoII), and intron-spanning fragments of three unlinked nuclear loci: triose-phosphate isomerase (Tpi), mannose-6-phosphate isomerase (Mpi) and cubitus interruptus (Ci) genes. A fifth gene, dopa decarboxylase (Ddc) produced sequence data likely to be from different duplicate loci in some of the taxa, and so was excluded. Mitochondrial and Tpi genealogies are consistent with reciprocal monophyly, whereas sympatric populations of the species in...

BMC Evolutionary Biology, 2007

Background: To understand speciation and the maintenance of taxa as separate entities, we need in... more Background: To understand speciation and the maintenance of taxa as separate entities, we need information about natural hybridization and gene flow among species. Results: Interspecific hybrids occur regularly in Heliconius and Eueides (Lepidoptera: Nymphalidae) in the wild: 26-29% of the species of Heliconiina are involved, depending on species concept employed. Hybridization is, however, rare on a per-individual basis. For one well-studied case of species hybridizing in parapatric contact (Heliconius erato and H. himera), phenotypically detectable hybrids form around 10% of the population, but for species in sympatry hybrids usually form less than 0.05% of individuals. There is a roughly exponential decline with genetic distance in the numbers of natural hybrids in collections, both between and within species, suggesting a simple "exponential failure law" of compatibility as found in some prokaryotes. Conclusion: Hybridization between species of Heliconius appears to be a natural phenomenon; there is no evidence that it has been enhanced by recent human habitat disturbance. In some well-studied cases, backcrossing occurs in the field and fertile backcrosses have been verified in insectaries, which indicates that introgression is likely, and recent molecular work shows that alleles at some but not all loci are exchanged between pairs of sympatric, hybridizing species. Molecular clock dating suggests that gene exchange may continue for more than 3 million years after speciation. In addition, one species, H. heurippa, appears to have formed as a result of hybrid speciation. Introgression may often contribute to adaptive evolution as well as sometimes to speciation itself, via hybrid speciation. Geographic races and species that coexist in sympatry therefore form part of a continuum in terms of hybridization rates or probability of gene flow. This finding concurs with the view that processes leading to speciation are continuous, rather than sudden, and that they are the same as those operating within species, rather than requiring special punctuated effects or complete allopatry. Although not qualitatively distinct from geographic races, nor "real" in terms of phylogenetic species concepts or the biological species concept, hybridizing species of Heliconius are stably distinct in sympatry, and remain useful groups for predicting morphological, ecological, behavioural and genetic characteristics.

Biological Journal of the Linnean Society, 2007

Phylogenetic information is useful in understanding the evolutionary history of adaptive traits. ... more Phylogenetic information is useful in understanding the evolutionary history of adaptive traits. Here, we present a well-resolved phylogenetic hypothesis for Heliconius butterflies and related genera. We use this tree to investigate the evolution of three traits, pollen feeding, pupal-mating behaviour and larval gregariousness. Phylogenetic relationships among 60 Heliconiina species (86% of the subtribe) were inferred from partial DNA sequences of the mitochondrial genes cytochrome oxidase I, cytochrome oxidase II and 16S rRNA, and fragments of the nuclear genes elongation factor-1α, apterous, decapentaplegic and wingless (3834 bp in total). The results corroborate previous hypotheses based on sequence data in showing that Heliconius is paraphyletic, with Laparus doris and Neruda falling within the genus, demonstrating a single origin for pollen feeding but with a loss of the trait in Neruda. However, different genes are not congruent in their placement of Neruda; therefore, monophy...

Molecular Biology and Evolution, 2002

Recent adaptive radiations provide excellent model systems for understanding speciation, but rapi... more Recent adaptive radiations provide excellent model systems for understanding speciation, but rapid diversification can cause problems for phylogenetic inference. Here we use gene genealogies to investigate the phylogeny of recent speciation in the heliconiine butterflies. We sequenced three gene regions, intron 3 (ഠ550 bp) of sex-linked triosephosphate isomerase (Tpi), intron 3 (ഠ450 bp) of autosomal mannose-phosphate isomerase (Mpi), and 1,603 bp of mitochondrial cytochrome oxidase subunits I and II (COI and COII), for 37 individuals from 25 species of Heliconius and related genera. The nuclear intron sequences evolved at rates similar to those of mitochondrial coding sequences, but the phylogenetic utility of introns was restricted to closely related geographic populations and species due to high levels of indel variation. For two sister species pairs, Heliconius erato-Heliconius himera and Heliconius melpomene-Heliconius cydno, there was highly significant discordance between the three genes. At mtDNA and Tpi, the hypotheses of reciprocal monophyly and paraphyly of at least one species with respect to its sister could not be distinguished. In contrast alleles sampled from the third locus, Mpi, showed polyphyletic relationships between both species pairs. In all cases, recent coalescence of mtDNA lineages within species suggests that polyphyly of nuclear genes is not unexpected. In addition, very similar alleles were shared between melpomene and cydno, implying recent gene flow. Our finding of discordant genealogies between genes is consistent with models of adaptive speciation with ongoing gene flow and highlights the need for multiple locus comparisons to resolve phylogeny among closely related species.

Heliconius melpomene is a mimetic butterfly that exhibits great geographic variation in color pat... more Heliconius melpomene is a mimetic butterfly that exhibits great geographic variation in color pattern. We present here a genetic linkage map based on analysis of genetic markers in 73 individuals from a single F 2 family, offspring of a cross between H. m. cythera from western Ecuador and H. m. melpomene from French Guiana. A novel ''three-step method'' is described for the analysis of dominant markers in an F 2 cross, using outbred parental strains and taking advantage of the lack of crossing over in female Lepidoptera. This method is likely to prove useful for future mapping studies in outbred species with crossing over restricted to one sex, such as the Lepidoptera and Drosophila. The resulting linkage map has 21 linkage groups corresponding to the 21 chromosomes of H. melpomene and includes 219 AFLP markers, 23 microsatellites, 19 singlecopy nuclear genes, and the color pattern switch genes Yb and Sb. The marker density is high, averaging .1/7 cM. The total map length is 1616 cM and the average chromosome length is 77 cM. The genome size of H. melpomene was estimated to be 292 Mb, giving a relationship of physical-to-map distance of 180 kb/cM. This map forms the basis for future comparative linkage analysis of color pattern evolution in Heliconius.

PLoS Genetics, 2010

Wing pattern evolution in Heliconius butterflies provides some of the most striking examples of a... more Wing pattern evolution in Heliconius butterflies provides some of the most striking examples of adaptation by natural selection. The genes controlling pattern variation are classic examples of Mendelian loci of large effect, where allelic variation causes large and discrete phenotypic changes and is responsible for both convergent and highly divergent wing pattern evolution across the genus. We characterize nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium (LD), and candidate gene expression patterns across two unlinked genomic intervals that control yellow and red wing pattern variation among mimetic forms of Heliconius erato. Despite very strong natural selection on color pattern, we see neither a strong reduction in genetic diversity nor evidence for extended LD across either patterning interval. This observation highlights the extent that recombination can erase the signature of selection in natural populations and is consistent with the hypothesis that either the adaptive radiation or the alleles controlling it are quite old. However, across both patterning intervals we identified SNPs clustered in several coding regions that were strongly associated with color pattern phenotype. Interestingly, coding regions with associated SNPs were widely separated, suggesting that color pattern alleles may be composed of multiple functional sites, conforming to previous descriptions of these loci as ''supergenes.'' Examination of gene expression levels of genes flanking these regions in both H. erato and its co-mimic, H. melpomene, implicate a gene with high sequence similarity to a kinesin as playing a key role in modulating pattern and provides convincing evidence for parallel changes in gene regulation across co-mimetic lineages. The complex genetic architecture at these color pattern loci stands in marked contrast to the single casual mutations often identified in genetic studies of adaptation, but may be more indicative of the type of genetic changes responsible for much of the adaptive variation found in natural populations.