Papers

2010
Baxter, S. W., Nadeau, N. J., Maroja, L. S., Wilkinson, P., Counterman, B. A., Dawson, A., Beltran, M., et al. (2010). Genomic hotspots for adaptation: the population genetics of Mullerian mimicry in the Heliconius melpomene clade. PLoS Genetics , 6(2), e1000794.Abstract

Wing patterning in Heliconius butterflies is a longstanding example of both Mullerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are "hotspots" for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by approximately 100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Mullerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.

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(Open Access) doi: 10.1371/journal.pgen.1000794.

Mallet, J. (2010). Group selection and the development of the biological species concept. Philosophical Transactions of the Royal Society , 365, 1853-1863.Abstract

The development of what became known as the biological species concept began with a paper by Theodosius Dobzhansky in 1935, and was amplified by a mutualistic interaction between Dobzhansky, Alfred Emerson and Ernst Mayr after the second world war. By the 1950s and early 1960s, these authors had developed an influential concept of species as coadapted genetic complexes at equilibrium. At this time many features of species were seen as group advantages maintained by selection to avoid breakdown of beneficial coadaptation and the 'gene pool'. Speciation thus seemed difficult. It seemed to require, more so than today, an external deus ex machina, such as allopatry or the founder effect, rather than ordinary within-species processes of natural selection, sexual selection, drift and gene flow. In the mid-1960s, the distinctions between group and individual selection were clarified. Dobzhansky and Mayr both understood the implications, but their views on species changed little. These group selectionist ideas now seem peculiar, and are becoming distinctly less popular today. Few vestiges of group selectionism and species-level adaptationism remain in recent reviews of speciation. One wonders how many of our own cherished views on evolution will seem as odd to future biologists.

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doi: 10.1098/rstb.2010.0040

Dasmahapatra, K. K., Elias, M., Hill, R. I., Hoffman, J. I., & Mallet, J. (2010). Mitochondrial DNA barcoding detects some species that are real, and some that are not. Molecular Ecology Resources , 10, 264-273.Abstract

Mimicry and extensive geographical subspecies polymorphism combine to make species in the ithomiine butterfly genus Mechanitis (Lepidoptera; Nymphalidae) difficult to determine. We use mitochondrial DNA (mtDNA) barcoding, nuclear sequences and amplified fragment length polymorphism (AFLP) genotyping to investigate species limits in this genus. Although earlier biosystematic studies based on morphology described only four species, mtDNA barcoding revealed eight well-differentiated haplogroups, suggesting the presence of four new putative 'cryptic species'. However, AFLP markers supported only one of these four new 'cryptic species' as biologically meaningful. We demonstrate that in this genus, deep genetic divisions expected on the basis of mtDNA barcoding are not always reflected in the nuclear genome, and advocate the use of AFLP markers as a check when mtDNA barcoding gives unexpected results.

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doi: 10.1111/j.1755-0998.2009.02763.x

de-Silva, D. L., Day, J. J., Elias, M., Willmott, K., Whinnett, A., & Mallet, J. (2010). Molecular phylogenetics of the neotropical butterfly subtribe Oleriina (Nymphalidae: Danainae: Ithomiini). Molecular Phylogenetics and Evolution , 55, 1032-1041.Abstract

The Oleriina is one of the most speciose subtribes of the neotropical nymphalid butterfly tribe Ithomiini. They are widely distributed across the Andes and Amazonian lowlands and like other ithomiines they are involved in complex mimicry rings. This subtribe is of particular interest because it contains the most diverse ithomiine genus, Oleria, as well as two genera, Megoleria and Hyposcada, that feed on hostplants not utilized elsewhere in the tribe. Here we present the first comprehensive species-level phylogeny for the Oleriina, representing 83% of recognised species in the group, and based on 6698bp from eight mitochondrial (mt) and nuclear (nc) genes. Topologies are largely congruent for ncDNA and the concatenated dataset and the genera Oleria, Hyposcada and Megoleria are recovered and well-supported, although strongly discordant genealogy between mtDNA and ncDNA suggest possible introgression among Hyposcada and Megoleria. A fourth clade containing the type species of Ollantaya is consistently recovered, and this recently synonymized name is resurrected. Clear subdivisions within Oleria separate the genus into four species groups, onega, amalda, makrena and aegle, which also correspond to differing biogeographic and elevation range characteristics. Unlike other ithomiine genera, the Oleriina show homogeneity in mimetic wing pattern, in sharp contrast to the emerging paradigm that mimetic shifts have enhanced diversification in the tribe. Our results show a potentially more important role for geographic isolation in the diversification of the Oleriina compared to other Ithomiini studied to date and provide a framework for more detailed biogeographical studies, in addition to a rare opportunity for comparative analyses with other neotropical groups.

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doi: 10.1016/j.ympev.2010.01.010

Mallet, J. (2010). Shift happens! Shifting balance and the evolution of diversity in warning colour and mimicry. Ecological Entomology , 35 (Suppl. 1), 90-104. REPRINT
Mallet, J. (2010). Why was Darwin’s view of species rejected by twentieth century biologists? Biology and Philosophy , 25, 497-527. REPRINT
2009
Sachs, J. D., Baillie, J. E. M., Sutherland, W. J., Armsworth, P. R., Ash, N., Beddington, J., Blackburn, T. M., et al. (2009). Policy forum: Biodiversity conservation and the Millennium Development Goals. Science , 325, 1502-1503.
Descimon, H., & Mallet, J. (2009). Bad species. In J Settele, TG Shreeve, M Konvicka, & V. H. Dyck (Ed.), Ecology of Butterflies in Europe (pp. 219-249) . Cambridge, Cambridge University Press. REPRINT
Mallet, J. (2009). Alfred Russel Wallace and the Darwinian species concept: his paper on the swallowtail butterflies (Papilionidae) of 1865. Gayana , 73 (suppl. 1), 35-47.Abstract

Soon after his return from the Malay Archipelago, Alfred Russel Wallace published one of his mostsignificant papers. The paper used butterflies of the family Papilionidae as a model system for testingevolutionary hypotheses, and included a revision of the Papilionidae of the region, as well as thedescription of some 20 new species. Wallace argued that the Papilionidae were the most advancedbutterflies, against some of his colleagues such as Bates and Trimen who had claimed that theNymphalidae were more advanced because of their possession of vestigial forelegs. In a very importantsection, Wallace laid out what is perhaps the clearest Darwinist definition of the differences betweenspecies, geographic subspecies, and local ‘varieties.’ He also discussed the relationship of thesetaxonomic categories to what is now termed ‘reproductive isolation.’ While accepting reproductiveisolation as a cause of species, he rejected it as a definition. Instead, species were recognized as formsthat overlap spatially and lack intermediates. However, this morphological distinctness argument breaksdown for discrete polymorphisms, and Wallace clearly emphasised the conspecificity of non-mimeticmales and female Batesian mimetic morphs in Papilio polytes, and also in P. memnon, on the groundsof reproductive continuity. Finally, Wallace detailed how natural selection explains various forms ofparallel evolution, including mimicry.

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Mallet, J. (2009). Ask the ecologist: Are genetic barcodes the magic tools we need to achieve a precise estimation of biodiversity in tropical ecosystems? What are the advantages and problems associated with this methodological proposal? Ecology Briefs. Informative Bulletin of the Centro Internacional de Ecología Tropical (CIET), Caracas , 1 3. REPRINT
Mallet, J., Meyer, A., Nosil, P., & Feder, J. L. (2009). Space, sympatry and speciation. Journal of Evolutionary Biology , 22, 2332-2341.Abstract

Sympatric speciation remains controversial. 'Sympatry' originally meant "in the same geographical area". Recently, evolutionists have redefined 'sympatric speciation' non-spatially to require panmixia (m = 0.5) between a pair of demes before onset of reproductive isolation. Although panmixia is a suitable starting point in models of speciation, it is not a useful definition of sympatry in natural populations, because it becomes virtually impossible to find or demonstrate sympatry in nature. The newer, non-spatial definition fails to address the classical debate about whether natural selection within a geographic overlap regularly causes speciation in nature, or whether complete geographic isolation is usually required. We therefore propose a more precise spatial definition by incorporating the population genetics of dispersal (or 'cruising range'). Sympatric speciation is considerably more likely under this spatial definition than under the demic definition, because distance itself has a powerful structuring effect, even over small spatial scales comparable to dispersal. Ecological adaptation in two-dimensional space often acts as a 'magic trait' that causes pleiotropic reductions of gene flow. We provide examples from our own research.

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doi: 10.1111/j.1420-9101.2009.01816.x

2008
Mallet, J. (2008). Mayr's view of Darwin: was Darwin wrong about speciation? Biological Journal of the Linnean Society , 95, 3-16. REPRINT
Mallet, J. (2008). Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philosophical Transactions of the Royal Society B-Biological Sciences , 363, 2971-2986.Abstract

Species are generally viewed by evolutionists as 'real' distinct entities in nature, making speciation appear difficult. Charles Darwin had originally promoted a very different uniformitarian view that biological species were continuous with 'varieties' below the level of species and became distinguishable from them only when divergent natural selection led to gaps in the distribution of morphology. This Darwinian view on species came under immediate attack, and the consensus among evolutionary biologists today appears to side more with the ideas of Ernst Mayr and Theodosius Dobzhansky, who argued 70 years ago that Darwin was wrong about species. Here, I show how recent genetic studies of supposedly well-behaved animals, such as insects and vertebrates, including our own species, have supported the existence of the Darwinian continuum between varieties and species. Below the level of species, there are well-defined ecological races, while above the level of species, hybridization still occurs, and may often lead to introgression and, sometimes, hybrid speciation. This continuum is evident, not only across vast geographical regions, but also locally in sympatry. The existence of this continuum provides good evidence for gradual evolution of species from ecological races and biotypes, to hybridizing species and, ultimately, to species that no longer cross. Continuity between varieties and species not only provides an excellent argument against creationism, but also gives insight into the process of speciation. The lack of a hiatus between species and ecological races suggests that speciation may occur, perhaps frequently, in sympatry, and the abundant intermediate stages suggest that it is happening all around us. Speciation is easy!

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doi: 10.1098/rstb.2008.0081

2007
Joron, M., Papa, R., Mallet, J., W. McMillan, O., & Jiggins, C. D. (2007). Conserved but flexible: Genetic control of mimicry in Heliconius butterfly wing patterns. Journal of Insect Science , 7 (1:29), 24. Publisher's VersionAbstract
It is now well known that convergent morphology can evolve via repeated recruitment of the same regulatory genes in different lineages. We here contrast three butterfly species, all classic examples of Müllerian mimicry. We use a genetic linkage map to show that a locus, Yb, controlling the presence of a yellow band in geographic races of H. melpomene maps precisely to the same location as the locus Cr, which has very similar phenotypic effects in its co-mimic H. erato. Furthermore, the same genomic location acts as a ’supergene’ determining multiple, sympatric morphs in a third species, H. numata, a species with a very different phenotypic appearance, whose many forms mimic different unrelated ithomiine butterflies in the genus Melinaea. Hence, a single locus from the multilocus colour pattern architecture in H. melpomene and H. erato appears to have gained control of the entire wing-pattern variability in H. numata, presumably as a result of selection for mimetic ’supergene’ polymorphism without intermediates. Our results imply that a conserved, yet relatively unconstrained mechanism underlying pattern switching can affect mimicry in radically different ways. We also show that adaptive evolution, both convergent and diversifying, can occur by the repeated involvement of the same genomic regions. In: Meeting Abstracts: 7th International Workshop on the Molecular Biology and Genetics of the Lepidoptera, August 20–26, 2006, Orthodox Academy of Crete, Kolympari, Crete, Greece
Anstead, J. A., Mallet, J., & Denholm, I. (2007). Temporal and spatial incidence of alleles conferring knockdown resistance to pyrethroids in the peach-potato aphid, Myzus persicae (Hemiptera: Aphididae), and their association with other insecticide resistance mechanisms. Bulletin of Entomological Research , 97, 243-252.
Beltrán, M., Jiggins, C. D., Brower, A. V. Z., Bermingham, E., & Mallet, J. (2007). Do pollen feeding and pupal-mating have a single origin in Heliconius? Inferences from multilocus sequence data. Biological Journal of the Linnean Society , 92, 221-239.Abstract

Phylogenetic information is useful in understanding the evolutionary history of adaptive traits. Here, we presenta well-resolved phylogenetic hypothesis for Heliconius butterflies and related genera. We use this tree toinvestigate 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 DNAsequences of the mitochondrial genes cytochrome oxidase I, cytochrome oxidase II and 16S rRNA, and fragmentsof the nuclear genes elongation factor-1a, apterous, decapentaplegic and wingless (3834 bp in total). The resultscorroborate previous hypotheses based on sequence data in showing that Heliconius is paraphyletic, with Laparusdoris and Neruda falling within the genus, demonstrating a single origin for pollen feeding but with a loss of thetrait in Neruda. However, different genes are not congruent in their placement of Neruda; therefore, monophylyof the pollen feeding species cannot be ruled out. There is also a highly supported monophyletic ‘pupal-matingclade’ suggesting that pupal mating behaviour evolved only once in the Heliconiina. Additionally, we observed atleast three independent origins for larval gregariousness from a solitary ancestor, showing that gregarious larvalbehaviour arose after warning coloration. © 2007 The Linnean Society of London, Biological Journal of theLinnean Society, 2007, 92, 221–239.

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Dasmahapatra, K. K., Silva-Vasquez, A., Chung, J. W., & Mallet, J. (2007). Genetic analysis of a wild-caught hybrid between non-sister Heliconius butterfly species. Biology Letters , 3 660-663.Abstract

Interspecific hybridization occurs regularly in wild Heliconius butterflies, although hybrid individuals are usually very rare. However, hybridization generally occurs only between the most closely related species. We report a rare naturally occurring hybrid between non-sister species and carry out the first genetic analysis of such distant hybridization. Mitochondrial and nuclear genes indicate that the specimen is an F1 hybrid between a female Heliconius ethilla and a male Heliconius melpomene, originating from a group of 13 species estimated to have diverged over 2.5 Myr ago. The presence of such distant natural hybrids, together with evidence for backcrossing, suggests that gene flow across species boundaries can take place long after speciation. Adaptive genes such as those involved in wing coloration could thus be widely shared among members of this highly mimetic genus.

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Mallet, J. (2007). Hybrid speciation. Nature , 446, 279-283.Abstract

Botanists have long believed that hybrid speciation is important, especially after chromosomal doubling (allopolyploidy). Until recently, hybridization was not thought to play a very constructive part in animal evolution. Now, new genetic evidence suggests that hybrid speciation, even without polyploidy, is more common in plants and also animals than we thought.

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Elias, M., Hill, R. I., Willmott, K. R., Dasmahapatra, K. K., Brower, A. V., Mallet, J., & Jiggins, C. D. (2007). Limited performance of DNA barcoding in a diverse community of tropical butterflies. Proceedings of the Royal Society , 274, 2881-9.Abstract

DNA 'barcoding' relies on a short fragment of mitochondrial DNA to infer identification of specimens. The method depends on genetic diversity being markedly lower within than between species. Closely related species are most likely to share genetic variation in communities where speciation rates are rapid and effective population sizes are large, such that coalescence times are long. We assessed the applicability of DNA barcoding (here the 5' half of the cytochrome c oxidase I) to a diverse community of butterflies from the upper Amazon, using a group with a well-established morphological taxonomy to serve as a reference. Only 77% of species could be accurately identified using the barcode data, a figure that dropped to 68% in species represented in the analyses by more than one geographical race and at least one congener. The use of additional mitochondrial sequence data hardly improved species identification, while a fragment of a nuclear gene resolved issues in some of the problematic species. We acknowledge the utility of barcodes when morphological characters are ambiguous or unknown, but we also recommend the addition of nuclear sequence data, and caution that species-level identification rates might be lower in the most diverse habitats of our planet.

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Mallet, J., Beltran, M., Neukirchen, W., & Linares, M. (2007). Natural hybridization in heliconiine butterflies: the species boundary as a continuum. BMC Evolutionary Biology , 7 28. Heliconiine hybrid databaseAbstract

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.

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