Guila Ganem

Rapid chromosomal evolution in island mice

Madeira is a small volcanic island in the Atlantic Ocean with steep mountains separating narrow valleys that are the only areas habitable by humans and their commensals. Here we show that house mice (Mus musculus domesticus ) on Madeira have an unexpected chromosomal diversity, the evolution of which is independent of adaptive processes, relying instead on geographic isolation and genetic drift.

Environmental genetics: Rapid chromosomal evolution in islandmice

Madeira is a small volcanic island in the Atlantic Ocean with steep mountains separating narrow valleys that are the only areas habitable by humans and their commensals. Here we show that house mice (Mus musculus domesticus ) on Madeira have an unexpected chromosomal diversity, the evolution of which is independent of adaptive processes, relying instead on geographic isolation and genetic drift.

Asymmetrical reproductive character displacement in the house mouse.

Our study addressed reproductive character displacement between two subspecies of the house mouse, Mus musculus musculus and Mus musculus domesticus that hybridize in Europe along a zone where selection against hybridization is known to occur. Based on a multi‐population approach, we investigated spatial patterns of divergence of mate preference in the two taxa. Mate preference was significantly higher in the contact zone than in allopatry in both subspecies, suggesting that reproductive character displacement occurs. Moreover, patterns of preference were stronger in M. m. musculus than in M. m. domesticus, indicating an asymmetrical divergence between the two. In the context of selection against hybridization, our results may provide empirical support for the hypothesis of reinforcement in a parapatric hybrid zone. We discuss factors that could explain the asymmetrical pattern of divergence and the possible impact of a unimodal structure on the maintenance of premating divergence between the two subspecies.

Strong premating divergence in a unimodal hybrid zone between two subspecies of the house mouse

Although selection against hybridization is expected to generate prezygotic divergence in unimodal hybrid zones, such a pattern has been seldom described. This study aims to better understand how prezygotic mechanisms may evolve in such zones. We investigated prezygotic divergence between populations of two subspecies of mice (Mus musculus musculus and M. m. domesticus) located at the edges of their unimodal hybrid zone in Denmark, and we developed an original multiple‐population choice‐test design, which allows assessment of within and between subspecies variation. Our study demonstrates that a strong assortative preference characterises one of the two subspecies (musculus) and that urinary signals are involved in this subspecies recognition. Taking into account the specific genetic and geographical characteristics of the Danish hybrid zone, we discuss the influence of the above pattern on its fate and the mechanisms that could have favoured this prezygotic divergence, among which the role of recombined populations constituting the core of the zone.

Molecular studies on the colonization of the Madeiran archipelago by house mice

To study the colonization history of the house mouse (Mus musculus domesticus) on the Madeiran archipelago, complete mitochondrial D‐loop sequences were obtained for 44 individuals from Madeira, Porto Santo and Ilhas Desertas. Altogether, 19 D‐loop haplotypes were identified which formed part of a single clade in a phylogeny incorporating haplotypes from elsewhere in the range of M. m. domesticus, indicating that the Madeiras were colonized from a single source. Similarities between the sequences found in the Madeiras and those in Scandinavia and northern Germany suggest that northern Europe was the source area, and there is the intriguing possibility that the Vikings may have accidentally brought house mice to the archipelago. However, there is no record of Vikings visiting the Madeiras; on historical grounds, Portugal is the most likely source area for Madeiran mice and further molecular data from Portugal are needed to rule out that possibility.

Variation in mate preference across a house mouse hybrid zone

Reproductive character displacement is known to occur at the borders of a secondary contact zone between the two European subspecies of the house mouse (in Jutland, Denmark), where selection against hybridization occurs. This study assessed patterns of mate preference in naturally occurring hybrids of the two subspecies. Mate odour choice was investigated in male and female mice sampled across the hybrid zone. Odour samples comprised urine (from the opposite sex to the test animal) obtained from populations geographically distant from the hybrid zone. Urine is known to carry subspecies recognition signals. The behavioural results changed across the hybrid zone, and were analysed by a model of clinal variation. This behavioural cline was compared with the allozyme cline across the same hybrid zone. Males on both sides of the hybrid zone showed an assortative preference, which shifted significantly and abruptly ∼10 km from the genetic centre of the hybrid zone on the Mus musculus musculus side. Directional preference was not detected in females, which could relate to variation in sexual receptivity. Our model indicates that the peculiar pattern of male preference could involve several genes and be characterized by mild to strong epistasis favouring the expression of M. m. domesticus-like preference over a large portion of the hybrid zone. This study may provide the first picture of the genetic determination of mate preference in a mammal.

Patterns of genic diversity and structure in a species undergoing rapid chromosomal radiation: an allozyme analysis of house mice from the Madeira archipelago

The chromosomal radiation of the house mouse in the island of Madeira most likely involved a human-mediated colonization event followed by within-island geographical isolation and recurrent episodes of genetic drift. The genetic signature of such processes was assessed by an allozyme analysis of the chromosomal races from Madeira. No trace of a decrease in diversity was observed suggesting the possibility of large founder or bottleneck sizes, multiple introductions and/or a high post-colonization expansion rate. The Madeira populations were more closely related to those of Portugal than to other continental regions, in agreement with the documented human colonization of the island. Such a Portuguese origin contrasts with a study indicating a north European source of the mitochondrial haplotypes present in the Madeira mice. This apparent discrepancy may be resolved if not one but two colonization events took place, an initial north European introduction followed by a later one from Portugal. Asymmetrical reproduction between these mice would have resulted in a maternal north European signature with a nuclear Portuguese genome. The extensive chromosomal divergence of the races in Madeira is expected to contribute to their genic divergence. However, there was no significant correlation between chromosomal and allozyme distances. This low apparent chromosomal impact on genic differentiation may be related to the short time since the onset of karyotypic divergence, as the strength of the chromosomal barrier will become significant only at later stages.

Sexual selection against natural hybrids may contribute to reinforcement in a house mouse hybrid zone

Sexual selection may hinder gene flow across contact zones when hybrid recognition signals are discriminated against. We tested this hypothesis in a unimodal hybrid zone between Mus musculus musculus and Mus musculus domesticus where a pattern of reinforcement was described and lower hybrid fitness documented. We presented mice from the border of the hybrid zone with a choice between opposite sex urine from the same subspecies versus hybrids sampled in different locations across the zone. While no preference was evidenced in domesticus mice, musculus males discriminated in favour of musculus signals and against hybrid signals. Remarkably, the pattern of hybrid unattractiveness did not vary across the hybrid zone. Moreover, allopatric populations tested in the same conditions did not discriminate against hybrid signals, indicating character displacement for signal perception or preference. Finally, habituation–discrimination tests assessing similarities between signals pointed out that hybrid signals differed from the parental ones. Overall, our results suggest that perception of hybrids as unattractive has evolved in border populations of musculus after the secondary contact with domesticus. We discuss the mechanisms involved in hybrid unattractiveness, and the potential impact of asymmetric sexual selection on the hybrid zone dynamics and gene flow between the two subspecies.

Urinary Volatile Molecules Vary in Males of the 2 European Subspecies of the House Mouse and Their Hybrids

Mice recognize other mice by identifying chemicals that confer a molecular signature to urinary marks. Such molecules may be involved in species recognition, and previous behavioral studies have related divergence of sexual preference between 2 subspecies of the house mouse (Mus musculus musculus and Mus musculus domesticus) to urinary odors. To characterize the differences between odors of males of the 2 subspecies and their first-generation offspring, the urinary volatile molecules were examined via gas chromatography coupled to mass spectrometry. Seven molecules were present in the samples from mice of at least one group. Their quantity varied among groups: M. m. domesticus showed a quantitatively richer panel of odorants in their urine when compared with M. m. musculus. The hybrids showed a more complex picture that was not directly related to one or the other parental subspecies. These quantitative differences may contribute to the specificity of the odorant bouquet of the 2 subspecies.

Phylogeny and adaptation shape the teeth of insular mice.

By accompanying human travels since prehistorical times, the house mouse dispersed widely throughout the world, and colonized many islands. The origin of the travellers determined the phylogenetic source of the insular mice, which encountered diverse ecological and environmental conditions on the various islands. Insular mice are thus an exceptional model to disentangle the relative role of phylogeny, ecology and climate in evolution. Molar shape is known to vary according to phylogeny and to respond to adaptation. Using for the first time a three-dimensional geometric morphometric approach, compared with a classical two-dimensional quantification, the relative effects of size variation, phylogeny, climate and ecology were investigated on molar shape diversity across a variety of islands. Phylogeny emerged as the factor of prime importance in shaping the molar. Changes in competition level, mostly driven by the presence or absence of the wood mouse on the different islands, appeared as the second most important effect. Climate and size differences accounted for slight shape variation. This evidences a balanced role of random differentiation related to history of colonization, and of adaptation possibly related to resource exploitation.