Papers

2009
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
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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2006
Joron, M., Papa, R., Beltran, M., Chamberlain, N., Mavarez, J., Baxter, S., Abanto, M., et al. (2006). A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biology , 4 e303.Abstract

We studied whether similar developmental genetic mechanisms are involved in both convergent and divergent evolution. Mimetic insects are known for their diversity of patterns as well as their remarkable evolutionary convergence, and they have played an important role in controversies over the respective roles of selection and constraints in adaptive evolution. Here we contrast three butterfly species, all classic examples of Mullerian mimicry. We used a genetic linkage map to show that a locus, Yb, which controls the presence of a yellow band in geographic races of Heliconius 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. H. numata is a species with a very different phenotypic appearance, whose many forms mimic different unrelated ithomiine butterflies in the genus Melinaea. Other unlinked colour pattern loci map to a homologous linkage group in the co-mimics H. melpomene and H. erato, but they are not involved in mimetic polymorphism in H. numata. Hence, a single region from the multilocus colour pattern architecture of 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. Although we cannot at this stage confirm the homology of the loci segregating in the three species, 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.

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Dasmahapatra, K. K., & Mallet, J. (2006). DNA barcodes: recent successes and future prospects. Heredity , 97, 254-255. REPRINT
Bull, V., Beltran, M., Jiggins, C. D., McMillan, W. O., Bermingham, E., & Mallet, J. (2006). Polyphyly and gene flow between non-sibling Heliconius species. BMC Biology , 4 11.Abstract

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 Mullerian 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.

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Mallet, J. (2006). What does Drosophila genetics tell us about speciation? Trends in Ecology and Evolution , 21, 386-93.Abstract

Studies of hybrid inviability, sterility and 'speciation genes' in Drosophila have given insight into the genetic changes that result in reproductive isolation. Here, I survey some extraordinary and important advances in Drosophila speciation research. However, 'reproductive isolation' is not the same as 'speciation', and this Drosophila work has resulted in a lopsided view of speciation. In particular, Drosophila are not always well-suited to investigating ecological and other selection-driven primary causes of speciation in nature. Recent advances have made use of far less tractable, but more charismatic organisms, such as flowering plants, vertebrates and larger insects. Work with these organisms has complemented Drosophila studies of hybrid unfitness to provide a more complete understanding of speciation.

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2005
Lamas, G., & Mallet, J. L. B. (2005). Case 3320. Papilio sapho Drury, 1782 (currently Heliconius sapho; Insecta, Lepidoptera): proposed conservation of the specific name. Bulletin of Zoological Nomenclature , 62, 21-24. REPRINT
Gourbiere, S., & Mallet, J. (2005). Has adaptive dynamics contributed to the understanding of adaptive and sympatric speciation? Journal of Evolutionary Biology , 18, 1201-1204. REPRINT
Mallet, J. (2005). Hybridization as an invasion of the genome. Trends in Ecology and Evolution , 20, 229-237.Abstract

Hybridization between species is commonplace in plants, but is often seen as unnatural and unusual in animals. Here, I survey studies of natural interspecific hybridization in plants and a variety of animals. At least 25% of plant species and 10% of animal species, mostly the youngest species, are involved in hybridization and potential introgression with other species. Species in nature are often incompletely isolated for millions of years after their formation. Therefore, much evolution of eventual reproductive isolation can occur while nascent species are in gene-flow contact, in sympatry or parapatry, long after divergence begins. Although the relative importance of geographic isolation and gene flow in the origin of species is still unknown, many key processes involved in speciation, such as 'reinforcement' of post-mating isolation by the evolution of assortative mating, will have ample opportunity to occur in the presence of continuing gene flow. Today, DNA sequence data and other molecular methods are beginning to show that limited invasions of the genome are widespread, with potentially important consequences in evolutionary biology, speciation, biodiversity, and conservation.

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Whinnett, A., Willmott, K. R., Brower, A. V. Z., Simpson, F., Lamas, G., & Mallet, J. (2005). Mitochondrial DNA provides an insight into the mechanisms driving diversification in the ithomiine butterfly Hyposcada anchiala (Lepidoptera: Nymphalidae, Ithomiinae). European Journal of Entomology , 102, 633-639.Abstract

Geographic subspecies of several ithomiine butterflies on the lower east Andean slopes display a black and orange“melanic tiger” aposematic wing pattern that occurs from Colombia to Bolivia, while geographically adjacent lowland subspeciestypically bear a coloured, “tiger” pattern. However, it is not clear whether subspecies with similar wing patterns in different regionshave arisen through independent events of convergent adaptation, possibly through parapatric differentiation, or result from allopatricdifferentiation, as proposed by the refuge hypothesis. Here, we examine geographic patterns of divergence in the widespreadand common ithomiine butterfly Hyposcada anchiala. We present phylogenetic hypotheses for 5 subspecies of H. anchiala, basedon 1567 bp mitochondrial DNA. All topologies indicated that a single switch in mimetic pattern best explained the wing patterningof the H. anchiala studied here. This finding suggests that the subspecies of H. anchiala studied here result from at least two stagesof differentiation, and is consistent with a single colonisation into a novel altitudinal zone coincident with a wing pattern switch, followedby subsequent divergence within, rather than across altitudinal zones. The subspecies divergences indicated diversificationswere consistent with the Pleistocene. Furthermore, the lowland subspecies were more recently derived than the montane taxa, in contrastto predictions of the “Andean species pump” hypothesis.

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