Catriona J. MacCallum's research while affiliated with Jagiellonian University and other places

This paper demonstrates the effect of habitat heterogeneity and a habitat preference on the genetic structure of a hybrid zone between the toads Bombina bombina and B. variegata (Anura: Discoglossidae); 1613 toads from 85 sites across a transect near Pešćenica, Croatia, were scored for five unlinked diagnostic allozyme markers. These were found to be largely concordant. Aside from minor systematic deviations, there was little variance in allele frequency among loci within sites. Yet the allele frequencies did not follow a smooth cline, but formed a mosaic in the center, such that neighboring sites could differ markedly in their enzyme score. A detailed ecological survey revealed a correlation between this pattern and habitat. In keeping with the typical breeding sites of the parental taxa, B. bombina-like hybrids were found more often in ponds, whereas B. variegata-like hybrids were more common in puddles. In addition, there was significant heterozygote deficit (FIS) and strong linkage disequilibrium (R), both of which were stronger on the B. bombina side of the transect, and stronger in puddles than ponds. Mark-recapture data showed: (1) that the animals disperse beyond the scale of the habitat pattern; (2) frequent turn-over of individuals within sites; and (3) nonrandom movement between two sites of different habitat type. We conclude that an active habitat preference must contribute to the observed association between marker alleles and habitat. As a consequence, there is incomplete mixing of the two gene pools, which could explain the high level of FIS and R. The asymmetry in these parameters may reflect asymmetry in the preference or in the distribution of habitats across the zone. We discuss the implications of habitat preference for the dynamics of hybrid zones.

This paper demonstrates the effect of habitat heterogeneity and a habitat preference on the genetic structure of a hybrid zone between the toads Bombina bombina and B. variegata (Anura: Discoglossidae); 1613 toads from 85 sites across a transect near Pešćenica, Croatia, were scored for five unlinked diagnostic allozyme markers. These were found to be largely concordant. Aside from minor systematic deviations, there was little variance in allele frequency among loci within sites. Yet the allele frequencies did not follow a smooth cline, but formed a mosaic in the center, such that neighboring sites could differ markedly in their enzyme score. A detailed ecological survey revealed a correlation between this pattern and habitat. In keeping with the typical breeding sites of the parental taxa, B. bombina-like hybrids were found more often in ponds, whereas B. variegata-like hybrids were more common in puddles. In addition, there was significant heterozygote deficit (FIS ) and strong linkage disequilibrium (R), both of which were stronger on the B. bombina side of the transect, and stronger in puddles than ponds. Mark-recapture data showed: (1) that the animals disperse beyond the scale of the habitat pattern; (2) frequent turn-over of individuals within sites; and (3) nonrandom movement between two sites of different habitat type. We conclude that an active habitat preference must contribute to the observed association between marker alleles and habitat. As a consequence, there is incomplete mixing of the two gene pools, which could explain the high level of FIS and R. The asymmetry in these parameters may reflect asymmetry in the preference or in the distribution of habitats across the zone. We discuss the implications of habitat preference for the dynamics of hybrid zones.

Observations on the means, variances, and covariances of quantitative traits across hybrid zones can give information similar to that from Mendelian markers. In addition, they can identify particular traits through which the cline is maintained. We describe a survey of six traits across the hybrid zone between Bombina bombina and Bombina variegata (Amphibia: Discoglossidae) near Pes6enica in Croatia. We obtained laboratory measuments of the belly pattern, skin thickness, mating call, skeletal form, egg size, and the developmental time of tadpoles. Although offspring from hybrid populations showed no evidence of reduced viability, a third of the F1 families failed completely, irre- spective of the direction of the cross. All traits differed significantly between the taxa. Clines in belly pattern, skin thickness, mating call, and skeletal form were closely concordant with clines in four diagnostic enzyme loci. However, the cline in developmental time was displaced towards bombina, and the cline in egg size was displaced towards variegata. This discordance could be because the traits are not inherited additively or because they are subject to different selection pressures. We favor the latter explanation in the case of developmental time. We show that moderate selection acting directly on a trait suffices to shift its position; rather stronger selection is needed to change its width appreciably. Within hybrid populations, there are significant associations among quantitative traits, and between traits and enzymes. Phenotypic variances also increase in hybrid populations. These observations can be explained by linkage disequilibria among the underlying loci. However, the average magnitude of the covariance between traits is about half that expected from the linkage disequilibria between enzyme loci. The discrepancy is not readily explained by nonadditive gene action. This puzzle is now unresolved and calls for further investigation.

Observations on the means, variances, and covariances of quantitative traits across hybrid zones can give information similar to that from Mendelian markers. In addition, they can identify particular traits through which the cline is maintained. We describe a survey of six traits across the hybrid zone between Bombina bombina and Bombina variegata (Amphibia: Discoglossidae) near Pešćenica in Croatia. We obtained laboratory measuments of the belly pattern, skin thickness, mating call, skeletal form, egg size, and the developmental time of tadpoles. Although offspring from hybrid populations showed no evidence of reduced viability, a third of the F1 families failed completely, irrespective of the direction of the cross. All traits differed significantly between the taxa. Clines in belly pattern, skin thickness, mating call, and skeletal form were closely concordant with clines in four diagnostic enzyme loci. However, the cline in developmental time was displaced towards bombina, and the cline in egg size was displaced towards variegata. This discordance could be because the traits are not inherited additively or because they are subject to different selection pressures. We favor the latter explanation in the case of developmental time. We show that moderate selection acting directly on a trait suffices to shift its position; rather stronger selection is needed to change its width appreciably. Within hybrid populations, there are significant associations among quantitative traits, and between traits and enzymes. Phenotypic variances also increase in hybrid populations. These observations can be explained by linkage disequilibria among the underlying loci. However, the average magnitude of the covariance between traits is about half that expected from the linkage disequilibria between enzyme loci. The discrepancy is not readily explained by nonadditive gene action. This puzzle is now unresolved and calls for further investigation.

Hybridizing taxa remain distinct for two main reasons. Natural selection acts against hybrids either because of their incompatible genome, or because of differential adaptation of the pure types across an environmental gradient. Here, we provide experimental evidence that the location of the Bombina (Anura: Discoglossidae) hybrid zone in Croatia is, at least in part, determined by differential adaptation. B. bombina typically breeds in permanent water in the lowland, whereas B. variegata reproduces in puddles at higher elevations. In a reciprocal translocation, pure bombina and variegata tadpoles were introduced in equal proportions into lowland pond enclosures and upland puddles. After three weeks, variegata exceeded bombina in survival and growth in both habitats. The effect was most pronounced in puddles, where the few surviving bombina tadpoles had hardly grown at all. In comparison to variegata, the smaller hatchlings of bombina grew relatively faster in ponds, but remained smaller in absolute terms. Nevertheless, B. bombina appears better adapted to ponds than to puddles. The mechanisms by which variegata is excluded from ponds remain to be demonstrated. These data show that habitat dependent selection prevents the invasion of bombina tadpole traits into the variegata gene pool. Given the strong linkage disequilibria in hybrid populations, differential selection on tadpoles may be sufficient to maintain the integrity of the two gene pools.