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Colliard et al. BMC Evolutionary Biology 2010, 10:232
http://www.biomedcentral.com/1471-2148/10/232

RESEARCH ARTICLE Open Access

Strong reproductive barriers in a narrow hybrid

zone of West-Mediterranean green toads (Bufo

viridis subgroup) with Plio-Pleistocene divergence

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Caroline Colliard , Alessandra Sicilia , Giuseppe Fabrizio Turrisi , Marco Arculeo , Nicolas Perrin , Matthias Stöck 1*
Abstract
Background: One key question in evolutionary biology deals with the mode and rate at which reproductive
isolation accumulates during allopatric speciation. Little is known about secondary contacts of recently diverged
anuran species. Here we conduct a multi-locus field study to investigate a contact zone between two lineages of
green toads with an estimated divergence time of 2.7 My, and report results from preliminary experimental crosses.
Results: The Sicilian endemic Bufo siculus and the Italian mainland-origin B. balearicus form a narrow hybrid zone
east of Mt. Etna. Despite bidirectional mtDNA introgression over a ca. 40 km North-South cline, no F 1 hybrids could
be found, and nuclear genomes display almost no admixture. Populations from each side of the contact zone
showed depressed genetic diversity and very strong differentiation (F ST = 0.52). Preliminary experimental crosses
point to a slightly reduced fitness in F 1 hybrids, a strong hybrid breakdown in backcrossed offspring (F 1 x parental,
with very few reaching metamorphosis) and a complete and early mortality in F 2 (F 1 xF 1 ).
Conclusion: Genetic patterns at the contact zone are molded by drift and selection. Local effective sizes are
reduced by the geography and history of the contact zone, B. balearicus populations being at the front wave of a
recent expansion (late Pleistocene). Selection against hybrids likely results from intrinsic genomic causes (disruption
of coadapted sets of genes in backcrosses and F 2 -hybrids), possibly reinforced by local adaptation (the ranges of
the two taxa roughly coincide with the borders of semiarid and arid climates). The absence of F 1 in the field might
be due to premating isolation mechanisms. Our results, show that these lineages have evolved almost complete
reproductive isolation after some 2.7 My of divergence, contrasting sharply with evidence from laboratory
experiments that some anuran species may still produce viable F 1 offspring after > 20 My of divergence.

Background distances among 50 species pairs, Wilson et al. [4]
One key question in evolutionary biology deals with the showed that frogs could still produce viable hybrids with
mode and rate at which reproductive isolation accumu- an average immunological distance of 7.4% (= ca. 21
lates during allopatric speciation [for overview: [1]]. My). Using Blair’s [5] crossing experiments in Bufo,
Johns and Avise [2] estimated the average mitochondrial Malone & Fontenot [6] showed the hatching success,
DNA (mtDNA)-based genetic distance between conge- the number of larvae produced, and the percentage of
neric species in amphibians to be > 7.0 My, suggesting tadpoles reaching metamorphosis to be inversely related
absence of natural hybridization in taxa of that age. A with genetic divergence, some metamorphosing off-
few major results on intrinsic reproductive isolation in spring being still produced with a distance of 8%
anurans come from artificial hybridization experiments. (mtDNA). All of these laboratory data suggest that
Sasa et al. [3] reported hybrid sterility or inviability in reproductive isolation increases gradually with phyloge-
46 frog species to be positively correlated with Nei’s netic distance, presumably driven by complex genomic
genetic distance (allozymes). Measuring albumin processes rather than by a few speciation genes, and
that very large time scales (in the order of tens of mil-
* Correspondence: matthias.stoeck@unil.ch lions of years) are required to achieve hybrid infertility
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Department of Ecology and Evolution, Biophore, University of Lausanne, or inviability.
CH-1015 Lausanne, Switzerland
© 2010 Colliard et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
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