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.2007 Feb 23:7:28.
doi: 10.1186/1471-2148-7-28.

Natural hybridization in heliconiine butterflies: the species boundary as a continuum

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Natural hybridization in heliconiine butterflies: the species boundary as a continuum

James Mallet et al. BMC Evol Biol..

Abstract

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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Figures

Figure 1
Figure 1
Phylogenetic relationships in the Heliconiina. The phylogenetic tree is based on a Bayesian/MCMC consensus tree obtained using a combination of mtDNA (CoI+CoII,16SRNA), and nuclear genes (elongation factor-1α,apterous,decapentaplegicandwingless) [30].*= Species known to hybridize with at least one other species in nature. The tree has been rooted usingBoloriaandAcraea. To give an idea of the relative time course of heliconiine evolution, HKY+gamma branch lengths have been estimated using the full likelihood rate-smoothing local molecular clock method of [101] on theCoI+CoIImitochondrial sequence data alone, after calibrating at the root with the estimated HKY+gamma average divergence between all heliconiines andAcraea(0.377).
Figure 2
Figure 2
Newly discovered or little-known interspecific hybrids inHeliconiusandEueides.a.Eueides isabella eva×E. vibilia vialis, male, hybrid no. 4;b.Eueides isabella eva×E. procula vulgiformis, male, hybrid no. 6;c.Heliconius numata aurora×H. melpomene malleti, female, hybrid no. 11;d.Heliconius hecale zeus×H. elevatus perchlorus, male, hybrid no. 16;e.Heliconius ethilla narcaea×H. besckei, female, hybrid no. 28;f.Heliconius numata superioris×H. melpomene meriana, male, hybrid no. 10;g.Heliconius melpomene cythera×H. cydno alithea, male, hybrid no. 34;h.Heliconius melpomene ssp. nov. ×H. cydno hermogenes, female, hybrid no. 65;i.H. erato petiverana×H. charithonia vasquezae, male, hybrid no. 158;j.Heliconius hecalesia octavia×H. hortense, male, hybrid no. 160. For further details, see Table 1 and Additional File 1. All hybrids are putative F1progeny of interspecies hybridization, exceptewhich is interpreted as a backcross toH. besckei. Photos:a,i– Sandra Knapp;b,g– James Mallet;c,f,j– Walter Neukirchen;d,e– Andrew Brower,h– Mauricio Linares.
Figure 3
Figure 3
A graphical representation of the species boundary. The numbers of natural hybrids known between pairs of species (from Table 1) are plotted on a logarithmic scale against the average uncorrected DNA divergence estimated from data for 1569 bp of mtDNA [30]. If backcrosses are also known from wild specimens, a halo around the point is shown. Comparisons reflect only species that have zones of overlap; average distance measures are given in Additional File 3. There are no known hybrids between species groups, and no estimates of divergence have been included for intergroup comparisons (NerudaandLaparusare here treated as part of themelpomene-cydno-silvaniform group to which they are closest in mtDNA divergence). A least-squares exponential fit of the species data alone is shown. (To display species pairs which lack known hybrids on the log-linear plot, they have been assigned 0.1 hybrids each, but the fitted line is based on a non-linear regression with untransformed data). Because the comparisons are non-independent, especially where branches of the same phylogeny or even the same species are used twice, a simple statistical analysis is not appropriate (under an assumption of independence, there is a highly significant negative correlation between in rates of hybridization and genetic distance:N= 180,P= 0.0022, although the proportion of the variance explained is not high,r2= 5%, because of the large number of species pairs for which no hybrids are known). Intraspecific hybridization also approximately fits this scheme; smaller square points in blue represent the equivalent numbers of intraspecific hybrids in world collections (not used in curve fitting). These were estimated by counting the numbers ofintraspecifichybrids (between morphologically divergent subspecies) in the 2001 catalogue of the W. Neukirchen collection, and dividing by the fraction of totalinterspecifichybrids in the Neukirchen collection over the total known worldwide.
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