Papers

2011
Mallet J, Wynne IR, Thomas CD. Hybridisation and climate change: brown argus butterflies in Britain (Polyommatus subgenus Aricia). Insect Conservation and Diversity. 2011;4 :192-199. REPRINT
De-Silva DL, VÁSquez AS, Mallet J. Selection for enemy-free space: eggs placed away from the host plant increase survival of a neotropical ithomiine butterfly. Ecological Entomology. 2011;36 :667-672.Abstract

1. The selection of an oviposition site by a phytophagous insect can depend
on many factors, including the risk of predation. Many species avoid predators by laying eggs where enemies searching host plants are unlikely to find them.
2. Females of the Peruvian butterfly, Oleria onega Hewitson (Lepidoptera:
Nymphalidae: Danainae: Ithomiini) lay most of their eggs (76 ± 9%) off the host plant, Solanum mite Ruiz & Pav. These off-host eggs may be laid up to 0.5 m from the nearest host-plant individual, on twigs or leaf litter, as well as on living plants of species unsuitable for larval food.
3. Disappearance of eggs on and off the host plant was recorded by transferring eggs laid in captivity to known locations in the wild and recording rates of disappearance before the larvae emerged. After 2 days, eggs on the host were significantly more likely to have disappeared compared to eggs laid elsewhere.
4. We conclude that a high risk of predation is a likely trigger that caused O. onega to evolve a behaviour of laying eggs off its host plant.

REPRINT
Hines HM, Counterman BA, Papa R, Albuquerque de Moura P, Cardoso MZ, Linares M, Mallet J, Reed RD, Jiggins CD, Kronforst MR, et al. A wing patterning gene redefines the mimetic history of Heliconius butterflies. Proceedings of the National Academy of Sciences, USA. 2011;108 :19666-19671.Abstract

The mimetic butterflies Heliconius erato and Heliconius melpomenehave undergone parallel radiations to form a near-identical patchworkof over 20 different wing-pattern races across the Neotropics.Previous molecular phylogenetic work on these radiations has suggestedthat similar but geographically disjunct color patterns arosemultiple times independently in each species. The neutral markersused in these studies, however, can move freely across color patternboundaries, and therefore might not represent the history ofthe adaptive traits as accurately as markers linked to color patterngenes. To assess the evolutionary histories across different loci, wecompared relationships among races within H. erato and within H.melpomene using a series of unlinked genes, genes linked to colorpattern loci, and optix, a gene recently shown to control red colorpatternvariation.We found that although unlinked genes partitionpopulations by geographic region, optix had a different history,structuring lineages by red color patterns and supporting a singleorigin of red-rayed patterns within each species. Genes closelylinked (80–250 kb) to optix exhibited only weak associations withcolor pattern. This study empirically demonstrates the necessity ofexamining phenotype-determining genomic regions to understandthe history of adaptive change in rapidly radiating lineages. Withthese refined relationships, we resolve a long-standing debateabout the origins of the races within each species, supporting thehypothesis that the red-rayed Amazonian pattern evolved recentlyand expanded, causing disjunctions of more ancestral patterns.

REPRINT
2010
Dasmahapatra KK, Lamas G, Simpson F, Mallet J. The anatomy of a 'suture zone' in Amazonian butterflies: a coalescent-based test for vicariant geographic divergence and speciation. Molecular Ecology. 2010;19 :4283-4301.Abstract

Attempts by biogeographers to understand biotic diversification in the Amazon have often employed contemporary species distribution patterns to support particular theories, such as Pleistocene rainforest refugia, rather than to test among alternative hypotheses. Suture zones, narrow regions where multiple contact zones and hybrid zones between taxa cluster, have been seen as evidence for past expansion of whole biotas that have undergone allopatric divergence in vicariant refuges. We used coalescent analysis of mutilocus sequence data to examine population split times in 22 pairs of geminate taxa in ithomiine and heliconiine butterflies. We test a hypothesis of simultaneous divergence across a suture zone in NE Peru. Our results reveal a scattered time course of diversification in this suture zone, rather than a tight cluster of split times. Additionally, we find rapid diversification within some lineages such as Melinaea contrasting with older divergence within lineages such as the Oleriina (Hyposcada and Oleria). These results strongly reject simple vicariance as a cause of the suture zone. At the same time, observed lineage effects are incompatible with a series of geographically coincident vicariant events which should affect all lineages similarly. Our results suggest that Pleistocene climatic forcing cannot readily explain this Peruvian suture zone. Lineage-specific biological traits, such as characteristic distances of gene flow or varying rates of parapatric divergence, may be of greater importance.

REPRINT

(Open Access) doi: 10.1111/j.1365-294X.2010.04802.x

Gourbiere S, Mallet J. Are species real? The shape of the species boundary with exponential failure, reinforcement, and the "missing snowball". Evolution. 2010;64 :1-24.Abstract

Under simple assumptions, the evolution of epistatic "Dobzhansky-Muller" incompatibilities between a pair of species should yield an accelerating decline of log overall reproductive compatibility--a "snowball" effect that might rapidly provide new species with "reality." Possible alternatives include: (1) simple exponential failure, giving a linear rate of log compatibility loss, and (2) "slowdown," likely during reinforcement in which mate choice evolves to prevent deleterious hybridization, yielding a decelerating log compatibility loss. In analyses of multiple datasets, we find little support for the snowball effect, except possibly in Lepidoptera hybrid viability. The snowball predicts a slow initial rate of incompatibility acquisition, with low initial variance; instead, highly variable compatibility is almost universally observed at low genetic distances. Another deviation from predictions is that reproductive isolation usually remains incomplete until long after speciation. These results do not disprove snowball compatibility decay, but can result if large deleterious effects are due to relatively few genetic changes, or if different types of incompatibility evolve at very different rates. On the other hand, data on Bacillus and Saccharomyces, as well as theories of chromosomal evolution, suggest that some kinds of incompatibility accumulate approximately linearly, without Dobzhansky-Muller effects. In microorganisms, linearity can result from direct negative effects of DNA sequence divergence on compatibility. Finally, a decelerating slowdown model is supported for sympatric Leptasterias starfish, and in Drosophila prezygotic isolation in sympatry but not allopatry, providing novel comparative evidence for reinforcement.

REPRINT

doi: 10.1111/j.1558-5646.2009.00844.x

Baxter SW, Nadeau NJ, Maroja LS, Wilkinson P, Counterman BA, Dawson A, Beltran M, Perez-Espona S, Chamberlain N, Ferguson L, et al. Genomic hotspots for adaptation: the population genetics of Mullerian mimicry in the Heliconius melpomene clade. PLoS Genetics. 2010;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.

REPRINT

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

Counterman BA, Araujo-Perez F, Hines HM, Baxter SW, Morrison CM, Lindstrom DP, Papa R, Ferguson L, Joron M, ffrench-Constant RH, et al. Genomic hotspots for adaptation: the population genetics of Mullerian mimicry in Heliconius erato. PLoS Genetics. 2010;6(2) :e1000796.Abstract

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.

REPRINT

doi: 10.1371/journal.pgen.1000796

Mallet J. Group selection and the development of the biological species concept. Philosophical Transactions of the Royal Society. 2010;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.

REPRINT

doi: 10.1098/rstb.2010.0040

Dasmahapatra KK, Elias M, Hill RI, Hoffman JI, Mallet J. Mitochondrial DNA barcoding detects some species that are real, and some that are not. Molecular Ecology Resources. 2010;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.

REPRINT

doi: 10.1111/j.1755-0998.2009.02763.x

de-Silva DL, Day JJ, Elias M, Willmott K, Whinnett A, Mallet J. Molecular phylogenetics of the neotropical butterfly subtribe Oleriina (Nymphalidae: Danainae: Ithomiini). Molecular Phylogenetics and Evolution. 2010;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.

REPRINT

doi: 10.1016/j.ympev.2010.01.010

Mallet J. Shift happens! Shifting balance and the evolution of diversity in warning colour and mimicry. Ecological Entomology. 2010;35 (Suppl. 1) :90-104. REPRINT
Mallet J. Why was Darwin’s view of species rejected by twentieth century biologists?. Biology and Philosophy. 2010;25 :497-527. REPRINT
2009
Sachs JD, Baillie JEM, Sutherland WJ, Armsworth PR, Ash N, Beddington J, Blackburn TM, Collen B, Gardiner B, Gaston KJ, et al. Policy forum: Biodiversity conservation and the Millennium Development Goals. Science. 2009;325 :1502-1503.
Descimon H, Mallet J. Bad species. In: J Settele, TG Shreeve, M Konvicka, Dyck VH Ecology of Butterflies in Europe. Cambridge: Cambridge University Press ; 2009. pp. 219-249. REPRINT
Mallet J. Alfred Russel Wallace and the Darwinian species concept: his paper on the swallowtail butterflies (Papilionidae) of 1865. Gayana. 2009;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. 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. 2009;1 :3. REPRINT
Mallet J, Meyer A, Nosil P, Feder JL. Space, sympatry and speciation. Journal of Evolutionary Biology. 2009;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.

REPRINT

doi: 10.1111/j.1420-9101.2009.01816.x

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

REPRINT

doi: 10.1098/rstb.2008.0081

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