Clinal analysis of a chromosomal hybrid zone in the house mouse

These studies centre on the 'Barcelona' karyotypic race of the western house mouse (Mus musculus domesticus), first described by Adolph & Klein (1981). This is one of many races within M. m. domesticus characterized by metacentric chromosomes that have originated by repeated Robertsonian fusions, with perhaps further modification by whole-arm reciprocal translocations. Data on 111 mice from 20 sites show that the race is centred 24 km to the west of Barcelona city and has a homozygous metacentric karyotype of 2n = 28 (3.8, 4.14, 5.15, 6.10, 9.11, 12.13). The race has a small range, and mice with the standard 40-acrocentric karyotype were caught only 30 km from the race centre. Throughout the area of occurrence of metacentrics there is polymorphism (i.e. presence of acrocentrics in the population), although all six metacentrics approach fixation close to the race centre. Thus, there is a hybrid zone between the Barcelona and standard races. The centres and widths of all clines (except 3.8) were determined. Likelihood ratio tests showed that most of the cline centres differed significantly in position (i.e. the clines were staggered) and the clines for metacentrics 6.10 and 9.11 were significantly narrower than those for 4.14, 5.15 and 12.13. Overall, the clines tended to be wider the further they were from the race centre. There are various possible explanations for this hybrid zone structure and further data are needed to distinguish between them.     

A hybrid zone comprising staggered chromosomal clines in the house mouse (Mus musculus domesticus).

In the vicinity of John o'Groats (Caithness, Scotland) there is a small karyotypic race of the house mouse (Mus musculus domesticus) characterized by a diploid number of 32 chromosomes, including the metacentrics 4.10, 9.12, 6.13 and 11.14. This race forms a hybrid zone with the standard British race (fully acrocentric chromosomes, 2n = 40). Although hybrid zones normally consist of several (or many) narrow character clines at the same position, this zone is unusual in that the chromosomal clines do not coincide. The cline for arm combination 11.14 is staggered relative to the 6.13 cline and both are separate from the clines for 4.10 and 9.12 (which may or may not coincide). A variety of explanations for the structure of the hybrid zone are discussed. It is possible that this may be a case of 'zonal raciation'.     

Natural hybridization between extremely divergent chromosomal races of the common shrew (Sorex araneus, Soricidae, Soricomorpha): hybrid zone in Siberia

Chromosomal races of the common shrew differ in sets of metacentric chromosomes and on contact may produce hybrids with extraordinarily complex configurations at meiosis I that are associated with reduced fertility. There is an expectation that these may be some of the most extreme tension zones available for study and therefore are of interest as potential sites for reproductive isolation. Here, we analyse one of these zones, between the Novosibirsk race (characterized by metacentrics go, hn, ik, jl, mp and qr) and the Tomsk race (metacentrics gk, hi, jl and mn and acrocentrics o, p, q and r), which form hybrids with a chain-of-nine (CIX) and a chain-of-three (CIII) configuration at meiosis I. At the Novosibirsk-Tomsk hybrid zone, the CIX chromosomes form clines of 8.53 km standardized width on average, whereas the cline for the CIII chromosomes was 52.83 km wide. The difference in these cline widths fits with the difference in meiotic errors expected with the CIX and CIII configuration, and we produce estimates of selection against hybrids with these types of configurations, which we relate to dispersal and age of the hybrid zone. The hybrid zone is located at the isocline at 200 m altitude above sea level; this relationship between the races and altitude is suggested at both coarse and fine scales. This indicates adaptive differences between the races that may in turn have been promoted by the chromosome differences. Thus, the extreme chromosomal divergence between the Novosibirsk and Tomsk may be associated with genic differentiation, but it is still striking that, despite the large chromosomal differences, reproductive isolation between the Novosibirsk and Tomsk races has not occurred.     

A comparison of five hybrid zones of the weta Hemideina thoracica (Orthoptera: Anostostomatidae): degree of cytogenetic differentiation fails to predict zone width

Abstract Tension zones are maintained by the interaction between selection against hybrids and dispersal of individuals. Investigating multiple hybrid zones within a single species provides the opportunity to examine differences in zone structure on a background of differences in extrinsic factors (e.g., age of the zone, ecology) or intrinsic factors (e.g., chromosomes). The New Zealand tree weta Hemideina thoracica comprises at least eight distinct chromosomal races with diploid numbers ranging from 2n = 11 (XO) to 2n = 23 (XO). Five independent hybrid zones were located that involve races differing from one another by a variety of chromosomal rearrangements. The predicted negative correlation between extent of karyotypic differentiation (measured in terms of both percent of genome and number of rearrangements) and zone width was not found. Conversely, the widest zones were those characterized by two chromosome rearrangements involving up to 35% of the genome. The narrowest zone occurred where the two races differ by a single chromosome rearrangement involving approximately 2% of the genome. The five estimates of chromosomal cline width ranged from 0.5 km to 47 km. A comparative investigation of cline width for both chromosomal and mitochondrial markers revealed a complex pattern of zone characteristics. Three of the five zones in this study showed cline concordance for the nuclear and cytoplasmic markers, and at two of the zones the clines were also coincident. Zones with the widest chromosomal clines had the widest mitochondrial DNA clines. It appears that, even within a single species, the extent of karyotypic differentiation between pairs of races is not a good predictor of the level of disadvantage suffered by hybrids.     

Behavioural discrimination among chromosomal races of the house mouse (Mus musculus domesticus)

This work is concerned with the extent of behavioural discrimination between three chromosomal races of the house mouse (the standard 40-chromosome race and a 32- and 36-chromosome races) found in the vicinity of a hybrid zone in northern Scotland. Mice were investigated for several elements of their social behaviour. Within-population dyadic encounters did not show consistent behavioural differences attributable to karyotype among five populations (two standard race, two 36-chromosome race, one 32-chromosome race). Between-population dyadic encounters revealed significant differences between three populations. The standard population examined appeared to be the most “open” to foreigners, the 32-chromosome population the most “closed” while the 36-chromosome mice displayed an intermediate response. Differences in behaviour displayed during between-population as compared to within-population dyadic encounters revealed the occurrence of behavioural discrimination between populations. The implication of these results on the dynamics of the hybrid zone are discussed.     

Non-metric morphological divergence in the western house mouse, Mus musculus domesticus, from the Barcelona chromosomal hybrid zone

The effect of hybridization on morphological variation was investigated in 120 western house mice, Mus musculus domesticus , from the hybrid zone between the Barcelona and standard chromosomal races. The incidence of 37 non-metric cranial traits was calculated for standard mice (2 n  = 40) and Barcelona-standard hybrids (2 n  = 27–39). Subsequent analyses were conducted on several karyological subgroups, established by grouping the animals according to either their diploid number or their degree of chromosomal heterozygosity. Results revealed no significant difference by sex, asymmetry, or geographical distance. Significant phenetic divergences were found between the karyotypes studied in relation to several variants. Differences were especially substantial between the standard race and hybrid mice, even with respect to those hybrids with karyotypes close to that of the standard race. Within the hybrids, the maximum divergence corresponded to the 28-chromosome homozygotes, chromosomally close to the Barcelona race, and to the heterozygotes with more than two fusions. Since differences in non-metric trait frequencies are generally considered a measure of genetic divergence, the results suggest the occurrence of a barrier to gene flow in the Barcelona hybrid zone. The decrease of genetic exchange between the chromosomally differentiated mice might be due to reduced fertility in hybrids, associated with chromosomal heterozygosity.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 313–322.     

Reproductive isolation between chromosomal races of the house mouse Mus musculus domesticus in a parapatric contact area revealed by an analysis of multiple unlinked loci

The house mouse, Mus musculus domesticus, exhibits a high level of chromosomal polymorphism because of the occurrence and fast fixation of Robertsonian fusions between telocentric chromosomes. For this reason, it has been considered a classical speciation model to analyse the role of the chromosomal changes in reproductive isolation. In this study, we analysed a parapatric contact area between two metacentric races in central Italy, the Cittaducale race (CD: 2n = 22) and the Ancarano race (ACR: 2n = 24), to estimate gene flow at the boundary. Hybrids between these two races show high levels of structural heterozygosity and are expected to be highly infertile. A sample of 88 mice from 14 sites was used. The mice were genotyped by means of eight microsatellite loci mapped in four different autosomal arms. The results show clear genetic differentiation between the CD and ACR races, as revealed by differences in allele frequencies, factorial correspondence analysis and indexes of genetic population (e.g. F(ST) and R(ST)) along the contact zone. The genetic differentiation between the races was further highlighted by assignation and clustering analyses, in which all the individuals were correctly assigned by their genotypes to the source chromosomal race. This result is particularly interesting in view of the absence of any geographical or ecological barrier in the parapatric contact zone, which occurs within a village. In these conditions, the observed genetic separation suggests an absence of gene flow between the races. The CD-ACR contact area is a rare example of a final stage of speciation between chromosomal races of rodents because of their chromosomal incompatibility.     

Narrow hybrid zone between Moscow and Western Dvina chromosomal races and specific features of population isolation in common shrew Sorex araneus (mammalia)

The contact zone between Moscow and Western Dvina chromosomal races of common shrew Sorex araneus L. at the south of the Valdai Hights was traced over a distance of 20 km. Within this, close to parapatric, contact zone of chromosomal races the width of sympatry zone was about 500 m (the narrowest among currently known hybrid zones), and the proportion of hybrids was 24.3%. It was shown that in bimodal hybrid zones between chromosomal races of common shrew the width of sympatry zones varied from 0.5 to 13 km. This width does not correlate with the cytogenetic features of the hybrids, and seems to be determined by competitive relations between the races. The hybrid proportion is determined by the type of hybrid heterozygosity, and decreased in the race sympatry zone from 33-40 to 21.5-25.2%. The decrease of the hybrid proportion can be associated with the abnormal fertility of either the first generation, or the backcross hybrids.     

Studies of mitochondrial DNA,allozyme and morphometric variation in a house mouse hybrid zone

An unusual chromosomal hybrid zone of the house mouse, Mus musculus domesticus, exists in Upper Valtellina, Northern Italy, consisting of four Robertsonian (Rb) races and the standard (all-acrocentric, or 2n = 40) race, all hybridizing freely within 10 km2. The hybrid zone in Valtellina provides an excellent opportunity to study the role of Rb fusions in reproductive isolation and speciation. This hybrid zone has already been well studied for the distribution of Rb fusions and the fertility of hybrids, but in order to understand the dynamics of the zone, a basic understanding of the origin and genetic similarity of the chromosomal races is necessary. This paper presents the results of three different methods of measuring genetic differentiation: multivariate analysis of morphological traits and analyses of allozyme variation and mitochondrial DNA sequences. The standard race is clearly distinguishable from the three Rb races by all three methods, but the Rb races are not distinguishable from one another. This provides strong evidence for our previous suggestions that the well-established Rb races in Valtellina are closely related, and that the standard race was introduced into the valley more recently from a distant source. The fact that the Rb races are indistinguishable is also consistent with our hypothesis that a within-village speciation event involving two of the races (Hauffe & Searle, 1992) was a recent occurrence. The low level of allozyme heterozygosity among the Rb races suggests that these populations are the products of at least one bottleneck. The present article substantially extends earlier studies and provides the first detailed morphological and molecular analysis of this complex hybrid zone.     

Narrow hybrid zone between Moscow and Western Dvina chromosomal races and specific features of population isolation in common shrew <Emphasis Type="Italic">Sorex araneus</Emphasis> (Mammalia)

The contact zone between Moscow and Western Dvina chromosomal races of common shrew Sorex araneus L. at the south of the Valdai Hights was traced over a distance of 20 km. Within this, close to parapatric, contact zone of chromosomal races the width of sympatry zone was about 500 m (the narrowest among currently known hybrid zones), and the proportion of hybrids was 24.3%. It was shown that in bimodal hybrid zones between chromosomal races of common shrew the width of sympatry zones varied from 0.5 to 13 km. This width does not correlate with the cytogenetic features of the hybrids, and seems to be determined by competitive relations between the races. The hybrid proportion is determined by the type of hybrid heterozygosity, and decreased in the race sympatry zone from 33–40 to 21.5–25.2%. The decrease of the hybrid proportion can be associated with the abnormal fertility of either the first generation, or the backcross hybrids.     

EXTREME KARYOTYPIC VARIATION IN A MUS MUSCULUS DOMESTICUS HYBRID ZONE: THE TOBACCO MOUSE STORY REVISITED

The Robertsonian fusion is a common chromosomal mutation among mammal species and is especially prevalent in the West European house mouse, Mus musculus domesticus. More than 40 races of the house mouse exist in Europe, including the famous “tobacco mouse” (Poschiavo race) of Val Poschiavo, Switzerland. Documented here is the discovery of an extreme case of karyotypic variation in the neighboring Upper Valtellina, Italy. In a 20-km stretch of the valley, 32 karyotypes were observed, including five chromosomal races and 27 hybrid types. One previously unknown race is reported, the “Mid Valtellina” race, with a diploid number of 2n = 24 and the Robertsonian fusions Rb(1.3), Rb(4.6), Rb(5.15), Rb(7.18), Rb(8.12), Rb(9.14), Rb(11.13), and Rb(16.17). The Poschiavo race (2n = 26), Upper Valtellina race (2n = 24), Lower Valtellina race (2n = 22) and all-acrocentric race (2n = 40) were also present. The races form a patchy distribution, which we term a “mottled hybrid zone.” Geographical position, isolation, extinction, recolonization, and selection against hybrids are all believed to be instrumental in the origin and evolution of this complex system. Previous studies of house mice from Upper Valtellina indicated that two of the races in the valley (the Upper Valtellina and Poschiavo races) may have speciated in the village of Migiondo. We discuss the possibility that there may have been a reinforcement event in this village.     

The structure of a chromosomal hybrid zone of house mice (Mus domesticus) in central Italy: cytogenetic analysis

Parapatric hybridization between the chromosomal race “CD” (2n = 22) and standard karyotype populations (2n = 40) of Mus domesticus occurs extensively in central Italy. The present paper reports the results of a ctogenetic surve on a transect crossin the hybrid zone north of Rome. No clinal variation in eitier diloid nuders and chromosome frequencies was found to occur in this area, and drift seems to be responsible for the observed atchy pattern of variation. The previous assumption of a strong fertility reduction in structuray heterozyous hybrids contrasts sharply with the width (32 km) of the zone and the average structural aeterozygosity of the hybrid poulations. It is suggested that fitness of structural heterozygotes in nature is not strongly aPfected as has been inferred from laboratory experiments. The results of this study are discussed in context together with the role of hybrid zones in chromosomal speciation in Mus domesticus.     

The complex hybrid zone between the Abisko and Sidensjö chromosome races of Sorex araneus in Sweden

Six chromosome races of the common shrew occur in Sweden, each with its characteristic arm combination of metacentric chromosomes. G-banded karyotypes were analysed from 201 common shrews in 14 localities of the northern hybrid zone in Sweden. Analyses from another 64 shrews from seven localities outside the hybrid zone w ere included for comparison. The shrews were classified with respect to karyotype into any of five categories: (1) Abisko race, (2) Sidensjö race, (3) hybrids between the parental races, (4) pseudohybrids (a type of hybrid), and (5) AT with all race-specific chromosomes (h, i, n, o, p, r) present as telocentrics. Hybrids occurred at a frequency close to Hardy-Weinberg expectation in the centre of the hybrid zone. Chromosome polymorphism of Robertsonian type was common and 43 different karyotypes were found among the specimens studied. The polymorphism involved six metacentric pairs in the Abisko and three in the Sidensjö race. The frequency of the Sidensjö race-specific metacentric hi decreased and the frequency of the Abisko race-specific hn increased from south-west to north-east along a transect across the hybrid zone. The number of race-specific telocentrics reached a peak 13 km north-east of the hi-hn cline centre. The estimated standardized cline width for chromosomes hi and hn was 16.0 km. The extension of the Sidensjö race is comparatively narrow [c. 50 km in the region of the investigation), and it is regarded to be a 'hybrid race' between the Uppsala race, which colonized Sweden from the south-west, and the Abisko race which arrived from the north-east after the most recent glaciation. The origin of the Sidensjö race is thus less than 10 000 years old, because earlier this area was covered by glacial ice.     

Linkage-dependent gene flow in a house mouse chromosomal hybrid zone

In the alpine valley of Valtellina there are two Robertsonian chromosomal races of house mouse, the Poschiavo (POS: 2n = 24-26) characterized by metacentric 8.12 and acrocentrics 2 and 10 and the Upper Valtellina (UV: 2n = 22-24) characterized by metacentrics 2.8 and 10.12. The races inhabit separate villages in the valley except in Sommacologna and Sondalo, where they both occur together with hybrids. A total of 179 mice from 16 villages were typed at 13 microsatellite loci. Seven of these loci were localized close to the centromeres of chromosomes 10 and 12, with the prediction that these regions on the race-specific chromosomes would be the most likely to experience a barrier to gene flow. The remaining six loci were localized at the telomeres of chromosomes 10 and 12 and at the centromeres of chromosomes that do not differ between the races. Substantial differences in allelic frequencies were found between the villages with POS and UV races at five of the loci at the centromeres of chromosomes 10 and 12 but at none of the other loci. These differences were not found to distinguish the two races in Sommacologna and Sondalo. Therefore, the centromeric regions of race-specific chromosomes do appear to experience a barrier to gene flow, although this can break down under intense interbreeding between the races. These results are considered in the context of Harrison's (1990) concept of the semipermeability of hybrid zones to gene exchange and in relation to parapatric speciation.     

Parapatric hybridization in the chromosomal speciation of the house mouse

Chromosomal races of the house mouse ( Mus domesticus ) occur extensively in Italy. The present paper reports results of studies on a hybrid zone in Central Italy on a chromosomal race with a 2 n = 22 karyotype and surrounding populations with a standard 2 n = 40 karyotype. Karyotypic and morphometric patterns of variation in this area are discussed in an attempt to contribute to an understanding of the chromosomal speciation in this species. Data are compared, where possible, with other findings on the same hybrid zone. Finally, it is suggested that changes in behavioural traits (inter-male aggression and female socio-sexual preferences) may help in promoting complete genetic isolation.     

Reproductive trait divergence and hybrid fertility patterns between chromosomal races of the house mouse in Tunisia: analysis of wild and laboratory-bred males and females

The divergence in reproductive features and hybrid fertility patterns between two chromosomal races (2 n  = 40, 40St, and 2 n  = 22, 22Rb) of the house mouse in Tunisia were re-assessed on a larger sample of wild and laboratory-bred individuals than studied hitherto. Results showed that litter sizes were significantly smaller in 40St than in 22Rb mice, contrary to previous analyses. This suggests that variation in litter size between the two chromosomal races is more likely related to selective and/or environmental factors acting locally than to interracial reproductive trait divergence. However, the significantly reduced litter size of F₁ hybrids compared with parental individuals was confirmed, and further highlighted a sex difference in hybrid infertility, as F₁ females produced fewer litters and of smaller size than males. Histological analyses of F₁ and backcrosses showed a breakdown of spermatogenesis in males and a significantly reduced primordial follicle pool in females. The degree of gametogenic dysfunction was not related to the level of chromosomal heterozygosity per se , but a significant effect of two Rb fusions on follicle number was observed in hybrid females. These results suggest that genetic incompatibilities contribute to primary gametogenic dysfunction in hybrids between the chromosomal races in Tunisia.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 407–416.     

Staggered clines in a hybrid zone between two chromosome races of the harvestman Gagrellopsis nodulifera (Arachnida: Opiliones)

We analyzed a hybrid zone between two chromosome races (2n = 16 and 2n = 22) of a Japanese harvestman, Gagrellopsis nodulifera Sato and Suzuki (Arachnida: Opiliones: Phalangiidae). The hybrid zone is located in the eastern part of Tottori Prefecture, western Honshu. The width of the zone is approximately 5 to 15 km. Three independent tandem fusions/fissions seem to be the main cause of the karyotypic differences between the parental races. Ten karyotypic variants were found in the hybrid zone. They differed by numbers of diploid chromosomes and trivalents detected in meiosis. In most of the collecting sites, karyotypic heterozygotes were less common than expected. A positive correlation was found between number of trivalents in a karyotype and its deficiency rate. In some sites, the deficit of heterozygous individuals was accompanied by an excess of the intermediate homozygotes. One of the three transects across the zone was studied in detail. We found that three types of single heterozygotes (2n = 17, 2n = 19 and 2n = 21) formed a series of successive, spatially separated peaks along the transect. Two types of intermediate homozygotes (2n = 18 and 2n = 20) were also spatially separated. The most parsimonious explanation of such a structure is the staggering of clines of three tandem (or Robertsonian) fusion/fission variants that differentiate the parental races caused by selection against multiple heterozygotes. Analysis of nondisjunction in single heterozygotes demonstrated that there was a strong interindividual variation in nondisjunction rate. The mean frequency of aneuploid MII in single heterozygotes was 0.10 +/- 0.03. Crossover exchanges in some critical regions of trivalents result in abnormal chromosomal configurations: chromosomes with unequal chromatids and dicentric chromosomes. Frequency of crossover-induced chromosomal abnormalities was low in single heterozygotes (approximately equal to 4%), and was unexpectedly high in the double heterozygotes (approximately equal to 15%). Selection against karyotypic heterozygotes is considered as a main evolutionary force responsible for the structuring of the hybrid zone. A positive association between diploid chromosome number and altitude was found. The race 2n = 16 tended to occupy lower altitudes than the 2n = 22 parental race. Differences in ecological preferences may be a result of previous adaptations to different environments in allopatry. A hypothesis concerning the origin and evolution of the hybrid zone is proposed.     

Raciation and speciation in house mice from the Alps: the role of chromosomes

There are at least 24 different karyotypic races of house mouse in the central Alps, each characterized by a different complement of ancestral acrocentric and derived metacentric chromosomes; altogether 55 different metacentric chromosomes have been described from the region. We argue that this chromosome variation largely arose in situ. If these races were to make contact, in most cases they would produce F1 hybrids with substantial infertility (sometimes complete sterility), due to nondisjunction and germ cell death associated with the formation of long-chain and/or ring configurations at meiosis. We present fertility estimates to confirm this for two particular hybrid types, one of which demonstrates male-limited sterility (in accordance with Haldane's Rule). As well as a model for speciation in allopatry, the Alpine mouse populations are of interest with regards speciation in parapatry: we discuss a possible reinforcement event. Raciation of house mice appears to have happened on numerous occasions within the central Alps. To investigate one possible source of new karyotypic races, we use a two-dimensional stepping stone model to examine the generation of recombinant races within chromosomal hybrid zones. Using field-derived ecological data and laboratory-derived fertility estimates, we show that hybrid karyotypic races can be generated at a reasonable frequency in simulations. Our model complements others developed for flowering plants that also emphasize the potential of chromosomal hybrid zones in generating new stable karyotypic forms.     

Electrophoretic analysis of a chromosomal hybrid zone in the grasshopper Podisma pedestris

We have made an extensive allozyme survey of 21 enzyme and protein loci in populations of the alpine grasshopper Podisma pedestris. This species occurs in two races, differing by a chromosomal fusion which separates the ancestral XO/XX race from a derived neo-XY race. These races also differ in DNA content, and hybrids between them have reduced viability. Electrophoresis reveals that the amount of genetic differentiation between these races is no greater than the variation among populations within each race. Both larger-scale surveys and a detailed survey of an area where the races hybridize, show that the chromosomal change is not correlated with gene frequency changes at any of the 21 loci studied. These findings are consistent with recently developed theory concerning the strength of the barrier to gene flow posed by a hybrid zone with characteristics such as those measured experimentally in Podisma. It is argued that hybrid zones in other species which involve allozymic differences do so because of stronger selection against hybrids rather than through mating isolation.     

DEVELOPMENTAL INSTABILITY IN WILD CHROMOSOMAL HYBRIDS OF THE HOUSE MOUSE

In wild populations of the house mouse from Tunisia, fluctuating asymmetry and character size of tooth traits were compared between chromosomal races (2n = 40, all acrocentric standard karyotype, and 2n = 22, with nine fixed Robertsonian fusions) and their natural hybrids. Developmental stability was impaired in hybrids compared to both parental groups. Because genetic divergence measured by allozyme markers was low, genomic incompatibilities were not expected between the chromosomal races. This suggests that differentiation of gene systems specifically involved in development may have occurred between the chromosomal races. Support for the latter was found in the study of character size which showed that the 2n = 22 mice had smaller teeth than either the hybrid or the standard mice. The study of Tunisian chromosomal races thus shows that chromosomal evolution may lead to important changes in coadapted gene systems without involving extensive genic differentiation.