Gene flow persists millions of years after speciation in Heliconius butterflies

<p>Abstract</p> <p>Background</p> <p>Hybridization, or the interbreeding of two species, is now recognized as an important process in the evolution of many organisms. However, the extent to which hybridization results in the transfer of genetic material across the species boundary (introgression) remains unknown in many systems, as does the length of time after initial divergence that the species boundary remains porous to such gene flow.</p> <p>Results</p> <p>Here I use genome-wide genotypic and DNA sequence data to show that there is introgression and admixture between the <it>melpomene</it>/<it>cydno </it>and silvaniform clades of the butterfly genus <it>Heliconius</it>, groups that separated from one another as many as 30 million generations ago. Estimates of historical migration based on 523 DNA sequences from 14 genes suggest unidirectional gene flow from the <it>melpomene</it>/<it>cydno </it>clade into the silvaniform clade. Furthermore, genetic clustering based on 520 amplified fragment length polymorphisms (AFLPs) identified multiple individuals of mixed ancestry showing that introgression is on-going.</p> <p>Conclusion</p> <p>These results demonstrate that genomes can remain porous to gene flow very long after initial divergence. This, in turn, greatly expands the evolutionary potential afforded by introgression. Phenotypic and species diversity in a wide variety of organisms, including <it>Heliconius</it>, have likely arisen from introgressive hybridization. Evidence for continuous gene flow over millions of years points to introgression as a potentially important source of genetic variation to fuel the evolution of novel forms.</p

Monarch butterflies use an environmentally sensitive, internal timer to control overwintering dynamics

The monarch butterfly (Danaus plexippus) complements its iconic migration with diapause, a hormonally controlled developmental programme that contributes to winter survival at overwintering sites. Although timing is a critical adaptive feature of diapause, how environmental cues are integrated with genetically‐determined physiological mechanisms to time diapause development, particularly termination, is not well understood. In a design that subjected western North American monarchs to different environmental chamber conditions over time, we modularized constituent components of an environmentally‐controlled, internal diapause termination timer. Using comparative transcriptomics, we identified molecular controllers of these specific diapause termination components. Calcium signalling mediated environmental sensitivity of the diapause timer, and we speculate that it is a key integrator of environmental condition (cold temperature) with downstream hormonal control of diapause. Juvenile hormone (JH) signalling changed spontaneously in diapause‐inducing conditions, capacitating response to future environmental condition. Although JH is a major target of the internal timer, it is not itself the timer. Epigenetic mechanisms are implicated to be the proximate timing mechanism. Ecdysteroid, JH, and insulin/insulin‐like peptide signalling are major targets of the diapause programme used to control response to permissive environmental conditions. Understanding the environmental and physiological mechanisms of diapause termination sheds light on fundamental properties of biological timing, and also helps inform expectations for how monarch populations may respond to future climate change.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/151901/1/mec15178_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/151901/2/mec15178.pd

Monarch butterflies use an environmentally sensitive, internal timer to control overwintering dynamics

The monarch butterfly (Danaus plexippus) complements its iconic migration with diapause, a hormonally controlled developmental programme that contributes to winter survival at overwintering sites. Although timing is a critical adaptive feature of diapause, how environmental cues are integrated with genetically‐determined physiological mechanisms to time diapause development, particularly termination, is not well understood. In a design that subjected western North American monarchs to different environmental chamber conditions over time, we modularized constituent components of an environmentally‐controlled, internal diapause termination timer. Using comparative transcriptomics, we identified molecular controllers of these specific diapause termination components. Calcium signalling mediated environmental sensitivity of the diapause timer, and we speculate that it is a key integrator of environmental condition (cold temperature) with downstream hormonal control of diapause. Juvenile hormone (JH) signalling changed spontaneously in diapause‐inducing conditions, capacitating response to future environmental condition. Although JH is a major target of the internal timer, it is not itself the timer. Epigenetic mechanisms are implicated to be the proximate timing mechanism. Ecdysteroid, JH, and insulin/insulin‐like peptide signalling are major targets of the diapause programme used to control response to permissive environmental conditions. Understanding the environmental and physiological mechanisms of diapause termination sheds light on fundamental properties of biological timing, and also helps inform expectations for how monarch populations may respond to future climate change.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/151901/1/mec15178_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/151901/2/mec15178.pd

Convocation

The origins of phenotypic variation within mimetic Heliconius butterflies have long fascinated biologists and naturalists. However, the evolutionary processes that have generated this extraordinary diversity remain puzzling. Here we examine intraspecific variation across Heliconius cydno diversification and compare this variation to that within the closely related H. melpomene and H. timareta radiations. Our data, which consist of both mtDNA and genome scan from nearly 2250 AFLP loci, reveal a complex history of differentiation and admixture at different geographic scales. Both mtDNA and AFLP phylogenies suggest that H. timareta and H. cydno are probably geographic extremes of the same radiation that likely diverged from H. melpomene during the Pliocene-Pleistocene boundary. MtDNA suggest that this radiation originated in Central America or the Northwestern region of South America, with a subsequent colonization of the eastern and western slopes of the Andes. Our genome-scan data indicate significant admixture among sympatric H. cydno/H.timareta and H. melpomene populations across the extensive geographic ranges of the two radiations. Within H. cydno, both mtDNA and AFLP data indicate significant population structure at local scales, with strong genetic differences even among adjacent H. cydno color pattern races. These genetic patterns highlight the importance of past geoclimatic events, intraspecific gene flow, and local population differentiation in the origin and establishment of new adaptive forms

Phylogeography and sexual macrocyst formation in the social amoeba Dictyostelium giganteum

<p>Abstract</p> <p>Background</p> <p>Microorganisms are ubiquitous, yet we are only beginning to understand their diversity and population structure. Social amoebae (Dictyostelia) are a diverse group of unicellular eukaryotic microbes that display a unique social behaviour upon starvation in which cells congregate and then some die to help others survive and disperse. The genetic relationships among co-occurring cells have a major influence on the evolution of social traits and recent population genetic analysis found extensive genetic variation and possible cryptic speciation in one dictyostelid species (<it>Dictyostelium purpureum</it>). To further characterize the interplay among genetic variation, species boundaries, social behaviour, and reproductive isolation in the Dictyostelia, we conducted phylogenetic analyses and mating experiments with the geographically widespread social amoeba <it>Dictyostelium giganteum</it>.</p> <p>Results</p> <p>We sequenced approximately 4,000 basepairs of the nuclear ribosomal DNA from 24 isolates collected from Texas, Michigan, Massachusetts, Virginia, and Wisconsin and identified 16 unique haplotypes. Analyses of the sequence data revealed very little genetic differentiation among isolates and no clear evidence of phylogenetic structure, although there was evidence for some genetic differentiation between the Massachusetts and Texas populations. These results suggest that sexual mating (macrocyst formation) is not likely to correlate with either genetic or geographical distance. To test this prediction, we performed 108 mating experiments and found no association between mating probability and genetic or geographical distance.</p> <p>Conclusions</p> <p><it>D. giganteum </it>isolates from across North America display little genetic variation, phylogeographic structure, and genetic differentiation among populations relative to the cryptic species observed within <it>D. purpureum</it>. Furthermore, variation that does exist does not predict the probability of mating among clones. These results have important implications for our understanding of speciation and social evolution in microbes.</p

DNA methylation is widespread across social Hymenoptera

SummaryGenomic imprinting is an epigenetic phenomenon by which the expression of a gene is influenced by the parent from which it is inherited. The evolutionary causes of imprinting are mysterious but it is likely to represent a form of within-genome conflict [1]. For instance, alleles inherited from the father and the mother will be in conflict over treatment of relatives to which they are differently related. In this context, natural selection may favor alleles with effects that differ depending on the allele's parental origin [1,2]. This ‘kinship theory of imprinting’ has been developed and tested largely in the context of parental provisioning of offspring [1,2]. Given their haplodiploid genetic system and interspecific variation in social traits, the Hymenoptera (ants, bees, and wasps) provide a large variety of novel contexts in which to examine this theory [2]. However, aside from evidence that imprinting determines sex in the parasitic wasp Nasonia vitripennis [3], and a QTL that appears to be paternally inherited in the honeybee [4], nothing is known about imprinting in this group of animals. Here we provide evidence that CpG methylation, a hallmark of imprinting, is ubiquitously present in social insects but the proportion of methylated sites varies substantially among species and developmental stages

Genome-wide introgression among distantly related Heliconius butterfly species

Background: Although hybridization is thought to be relatively rare in animals, the raw genetic material introduced via introgression may play an important role in fueling adaptation and adaptive radiation. The butterfly genus Heliconius is an excellent system to study hybridization and introgression but most studies have focused on closely related species such as H. cydno and H. melpomene. Here we characterize genome-wide patterns of introgression between H. besckei, the only species with a red and yellow banded 'postman' wing pattern in the tiger-striped silvaniform clade, and co-mimetic H. melpomene nanna. Results: We find a pronounced signature of putative introgression from H. melpomene into H. besckei in the genomic region upstream of the gene optix, known to control red wing patterning, suggesting adaptive introgression of wing pattern mimicry between these two distantly related species. At least 39 additional genomic regions show signals of introgression as strong or stronger than this mimicry locus. Gene flow has been on-going, with evidence of gene exchange at multiple time points, and bidirectional, moving from the melpomene to the silvaniform clade and vice versa. The history of gene exchange has also been complex, with contributions from multiple silvaniform species in addition to H. besckei. We also detect a signature of ancient introgression of the entire Z chromosome between the silvaniform and melpomene/cydno clades. Conclusions: Our study provides a genome-wide portrait of introgression between distantly related butterfly species. We further propose a comprehensive and efficient workflow for gene flow identification in genomic data sets

Comparative population genetics of mimetic Heliconius butterflies in an endangered habitat; Brazil's Atlantic Forest

<p>Abstract</p> <p>Background</p> <p>Brazil's Atlantic Forest is a biodiversity hotspot endangered by severe habitat degradation and fragmentation. Habitat fragmentation is expected to reduce dispersal among habitat patches resulting in increased genetic differentiation among populations. Here we examined genetic diversity and differentiation among populations of two <it>Heliconius </it>butterfly species in the northern portion of Brazil's Atlantic Forest to estimate the potential impact of habitat fragmentation on population connectivity in butterflies with home-range behavior.</p> <p>Results</p> <p>We generated microsatellite, AFLP and mtDNA sequence data for 136 <it>Heliconius erato </it>specimens from eight collecting locations and 146 <it>H. melpomene </it>specimens from seven locations. Population genetic analyses of the data revealed high levels of genetic diversity in <it>H. erato </it>relative to <it>H. melpomene</it>, widespread genetic differentiation among populations of both species, and no evidence for isolation-by-distance.</p> <p>Conclusions</p> <p>These results are consistent with the hypothesis that the extensive habitat fragmentation along Brazil's Atlantic Forest has reduced dispersal of <it>Heliconius </it>butterflies among neighboring habitat patches. The results also lend support to the observation that fine-scale population genetic structure may be common in <it>Heliconius</it>. If such population structure also exists independent of human activity, and has been common over the evolutionary history of <it>Heliconius </it>butterflies, it may have contributed to the evolution of wing pattern diversity in the genus.</p

Gene flow and the genealogical history of Heliconius heurippa.

BACKGROUND: The neotropical butterfly Heliconius heurippa has a hybrid colour pattern, which also contributes to reproductive isolation, making it a likely example of hybrid speciation. Here we used phylogenetic and coalescent-based analyses of multilocus sequence data to investigate the origin of H. heurippa. RESULTS: We sequenced a mitochondrial region (CoI and CoII), a sex-linked locus (Tpi) and two autosomal loci (w and sd) from H. heurippa and the putative parental species, H. cydno and H. melpomene. These were analysed in combination with data from two previously sequenced autosomal loci, Dll and Inv. H. heurippa was monophyletic at mtDNA and Tpi, but showed a shared distribution of alleles derived from both parental lineages at all four autosomal loci. Estimates of genetic differentiation showed that H. heurippa is closer to H. cydno at mtDNA and three autosomal loci, intermediate at Tpi, and closer to H. melpomene at Dll. Using coalescent simulations with the Isolation-Migration model (IM), we attempted to establish the incidence of gene flow in the origin of H. heurippa. This analysis suggested that ongoing introgression is frequent between all three species and variable in extent between loci. CONCLUSION: Introgression, which is a necessary precursor of hybrid speciation, seems to have also blurred the coalescent history of these species. The origin of Heliconius heurippa may have been restricted to introgression of few colour pattern genes from H. melpomene into the H. cydno genome, with little evidence of genomic mosaicism.RIGHTS : This article is licensed under the BioMed Central licence at http://www.biomedcentral.com/about/license which is similar to the 'Creative Commons Attribution Licence'. In brief you may : copy, distribute, and display the work; make derivative works; or make commercial use of the work - under the following conditions: the original author must be given credit; for any reuse or distribution, it must be made clear to others what the license terms of this work are

Sex Chromosome Mosaicism and Hybrid Speciation among Tiger Swallowtail Butterflies

Hybrid speciation, or the formation of a daughter species due to interbreeding between two parental species, is a potentially important means of diversification, because it generates new forms from existing variation. However, factors responsible for the origin and maintenance of hybrid species are largely unknown. Here we show that the North American butterfly Papilio appalachiensis is a hybrid species, with genomic admixture from Papilio glaucus and Papilio canadensis. Papilio appalachiensis has a mosaic phenotype, which is hypothesized to be the result of combining sex-linked traits from P. glaucus and P. canadensis. We show that P. appalachiensis' Z-linked genes associated with a cooler thermal habitat were inherited from P. canadensis, whereas its W-linked mimicry and mitochondrial DNA were inherited from P. glaucus. Furthermore, genome-wide AFLP markers showed nearly equal contributions from each parental species in the origin of P. appalachiensis, indicating that it formed from a burst of hybridization between the parental species, with little subsequent backcrossing. However, analyses of genetic differentiation, clustering, and polymorphism based on molecular data also showed that P. appalachiensis is genetically distinct from both parental species. Population genetic simulations revealed P. appalachiensis to be much younger than the parental species, with unidirectional gene flow from P. glaucus and P. canadensis into P. appalachiensis. Finally, phylogenetic analyses, combined with ancestral state reconstruction, showed that the two traits that define P. appalachiensis' mosaic phenotype, obligatory pupal diapause and mimicry, evolved uniquely in P. canadensis and P. glaucus, respectively, and were then recombined through hybridization to form P. appalachiensis. These results suggest that natural selection and sex-linked traits may have played an important role in the origin and maintenance of P. appalachiensis as a hybrid species. In particular, ecological barriers associated with a steep thermal cline appear to maintain the distinct, mosaic genome of P. appalachiensis despite contact and occasional hybridization with both parental species