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Location of an X-linked factor causing sterility in male hybrids of Drosophila simulans and D. mauritiana.

We report the first mapping of a genetic factor responsible for reproductive isolation: a small segment of genome strongly affecting sperm motility in hybrids between the sibling species Drosophila simulans and D. mauritiana. Maximum-likelihood analysis of data from ten generations of backcrossing places this factor at 1.1 +/- 0.2 map units from the forked locus, at position 54.9 +/- 0.2 or 57.1 +/- 0.2 on the X chromosome.

Animals↗

Genetic analysis of X-linked sterility in hybrids between three sibling species of Drosophila.

Three morphological markers (yellow, miniature, and forked) are used to map the location of X-chromosome segments causing male sterility in Drosophila simulans/D. mauritiana and D. simulans/D. sechellia hybrids. In both hybridizations at least three sections of the chromosome contain genes with substantial effects on sterility. This represents the maximum genetic divergence detectable with the three markers, suggesting that the X chromosome contains many loci affecting postzygotic reproductive isolation. The tight linkage between some markers and "sterility loci" may be useful in localizing and later cloning genes important in speciation.

Animals↗

Fertility estimates in the Tunisian all-acrocentric and Robertsonian populations of the house mouse and their chromosomal hybrids.

The reproductive features of wild all-acrocentric and 2n = 22 Robertsonian (Rb) house mice (M. m. domesticus) from Tunisia were studied. The aim was to examine the possibility of a reproductive selective advantage associated with chromosomal change as well as to measure the effect of heterozygosity for a large number of Rb fusions on the fertility of hybrids. Results showed that litter sizes were significantly smaller in Rb than in all-acrocentric mice. This difference, which may represent a favourable demographic strategy related to the habitat segregation observed in the Tunisian mice, needs to be studied further. The F1 hybrids between the two chromosomal races showed a significantly reduced reproductive success and litter size (respectively, 53 per cent and 60 per cent less than either parental race). Analysis of the testicular histology of F1 and backcross males showed in some cases a breakdown of spermatogenesis. The degree of this disturbance was not related to the level of chromosomal heterozygosity suggesting that genetic incompatibilities between the two genomes might be involved. The strong reduction in fertility measured in these hybrids represents a reproductive isolating mechanism effectively reducing gene flow between the all-acrocentric and 22Rb mice populations of Tunisia.

Analysis of Variance↗

Genetic variability of the interpulse interval of courtship song among some European populations of Drosophila melanogaster.

The interpulse interval of the courtship song of Drosophila melanogaster is a character which may play a significant role in mating success and reproductive isolation. Here we examine the variability of interpulse interval among replicated laboratory strains of D. melanogaster. There is no significant variation among populations of different geographical origin. This suggests that interpulse interval is subject to strong selection, as the populations are known to differ for other characters. One population, however, was sufficiently different to allow a genetic analysis. Reciprocal F1s and backcrosses implied that the variance was predominantly additive and autosomal. Possible sources of selection on interpulse interval are discussed.

Animals↗

Mitochondrial DNA differentiation among geographical populations of Pronolagus rupestris, Smith's red rock rabbit (Mammalia: Lagomorpha).

Geographical genetic population structure was determined for an endemic African leporid, Smith's red rock rabbit, Pronolagus rupestris. Restriction fragment length polymorphism analysis of mitochondrial DNA from 55 specimens revealed 32 distinct material lineages for the population sampled. The data show two major genetic assemblages separated by a mean sequence divergence of 7.94 per cent (+/- 1.40 per cent) and provide little support for the continued recognition of most of the described subspecies. The south-eastern assemblage is confined to the mountain ranges comprising the Great Escarpment of South Africa, while the north-western assemblage is not so tightly constrained. With the possible exception of elevation, no readily apparent ecological or topographical barrier could be identified which delimits the two mitochondrial clades. The sequence divergence separating the south-eastern and north western P. rupestris clades is high, and approximates the interspecific sequence divergences detected between P. rupestris and other Pronolagus species. The two P. rupestris clades are parapatric for part of their distribution, and the absence of shared mtDNA lineages is consistent with the hypothesis that the two populations are reproductively isolated from each other. We provisionally interpret this to reflect the presence of two hitherto undetected biological species in what has conventionally been recognized as a single taxon, P. rupestris.

Animals↗

Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila.

Speciation--the splitting of one species into two--occurs by the evolution of any of several forms of reproductive isolation between taxa, including the intrinsic sterility and inviability of hybrids. Abundant evidence shows that these hybrid fitness problems are caused by incompatible interactions between loci: new alleles that become established in one species are sometimes functionally incompatible with alleles at interacting loci from another species. However, almost nothing is known about the genes involved in such hybrid incompatibilities or the evolutionary forces that drive their divergence. Here we identify a gene that causes epistatic inviability in hybrids between two fruitfly species, Drosophila melanogaster and D. simulans. Our population genetic analysis reveals that this gene--which encodes a nuclear pore protein--evolved by positive natural selection in both species' lineages. These results show that a lethal hybrid incompatibility has evolved as a by-product of adaptive protein evolution.

Adaptation, Biological↗

Speciation by host switch in brood parasitic indigobirds.

A growing body of empirical and theoretical work supports the plausibility of sympatric speciation, but there remain few examples in which all the essential components of the process are well understood. The African indigobirds Vidua spp. are host-specific brood parasites. Indigobird nestlings are reared along with host young, and mimic the mouth markings of their respective hosts. As adults, male indigobirds mimic host song, whereas females use these songs to choose both their mates and the nests they parasitize. These behavioural mechanisms promote the cohesion of indigobird populations associated with a given host species, and provide a mechanism for reproductive isolation after a new host is colonized. Here we show that all indigobird species are similar genetically, but are significantly differentiated in both mitochondrial haplotype and nuclear allele frequencies. These data support a model of recent sympatric speciation. In contrast to the cuckoo Cuculus canorus, in which only female lineages are faithful to specific hosts, host switches have led to speciation in indigobirds because both males and females imprint on their hosts.

Africa↗

Harmonic-hopping in Wallacea's bats.

Evolutionary divergence between species is facilitated by ecological shifts, and divergence is particularly rapid when such shifts also promote assortative mating. Horseshoe bats are a diverse Old World family (Rhinolophidae) that have undergone a rapid radiation in the past 5 million years. These insectivorous bats use a predominantly pure-tone echolocation call matched to an auditory fovea (an over-representation of the pure-tone frequency in the cochlea and inferior colliculus) to detect the minute changes in echo amplitude and frequency generated when an insect flutters its wings. The emitted signal is the accentuated second harmonic of a series in which the fundamental and remaining harmonics are filtered out. Here we show that three distinct, sympatric size morphs of the large-eared horseshoe bat (Rhinolophus philippinensis) echolocate at different harmonics of the same fundamental frequency. These morphs have undergone recent genetic divergence, and this process has occurred in parallel more than once. We suggest that switching harmonics creates a discontinuity in the bats' perception of available prey that can initiate disruptive selection. Moreover, because call frequency in horseshoe bats has a dual function in resource acquisition and communication, ecological selection on frequency might lead to assortative mating and ultimately reproductive isolation and speciation, regardless of external barriers to gene flow.

Acoustics↗

Host shift to an invasive plant triggers rapid animal hybrid speciation.

Speciation in animals is almost always envisioned as the split of an existing lineage into an ancestral and a derived species. An alternative speciation route is homoploid hybrid speciation in which two ancestral taxa give rise to a third, derived, species by hybridization without a change in chromosome number. Although theoretically possible it has been regarded as rare and hence of little importance in animals. On the basis of molecular and chromosomal evidence, hybridization is the best explanation for the origin of a handful of extant diploid bisexual animal taxa. Here we report the first case in which hybridization between two host-specific animals (tephritid fruitflies) is clearly associated with the shift to a new resource. Such a hybrid host shift presents an ecologically robust scenario for animal hybrid speciation because it offers a potential mechanism for reproductive isolation through differential adaptation to a new ecological niche. The necessary conditions for this mechanism of speciation are common in parasitic animals, which represent much of animal diversity. The frequency of homoploid hybrid speciation in animals may therefore be higher than previously assumed.

Adaptation, Physiological↗

Sympatric speciation in Nicaraguan crater lake cichlid fish.

Sympatric speciation, the formation of species in the absence of geographical barriers, remains one of the most contentious concepts in evolutionary biology. Although speciation under sympatric conditions seems theoretically possible, empirical studies are scarce and only a few credible examples of sympatric speciation exist. Here we present a convincing case of sympatric speciation in the Midas cichlid species complex (Amphilophus sp.) in a young and small volcanic crater lake in Nicaragua. Our study includes phylogeographic, population-genetic (based on mitochondrial DNA, microsatellites and amplified fragment length polymorphisms), morphometric and ecological analyses. We find, first, that crater Lake Apoyo was seeded only once by the ancestral high-bodied benthic species Amphilophus citrinellus, the most common cichlid species in the area; second, that a new elongated limnetic species (Amphilophus zaliosus) evolved in Lake Apoyo from the ancestral species (A. citrinellus) within less than approximately 10,000 yr; third, that the two species in Lake Apoyo are reproductively isolated; and fourth, that the two species are eco-morphologically distinct.

Animals↗

Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts.

A whole-genome duplication occurred in a shared ancestor of the yeast species Saccharomyces cerevisiae, Saccharomyces castellii and Candida glabrata. Here we trace the subsequent losses of duplicated genes, and show that the pattern of loss differs among the three species at 20% of all loci. For example, several transcription factor genes, including STE12, TEC1, TUP1 and MCM1, are single-copy in S. cerevisiae but are retained in duplicate in S. castellii and C. glabrata. At many loci, different species have lost different members of a duplicated gene pair, so that 4-7% of single-copy genes compared between any two species are not orthologues. This pattern of gene loss provides strong evidence for speciation through a version of the Bateson-Dobzhansky-Muller mechanism, in which the loss of alternative copies of duplicated genes leads to reproductive isolation. We show that the lineages leading to the three species diverged shortly after the whole-genome duplication, during a period of precipitous gene loss. The set of loci at which single-copy paralogues are retained is biased towards genes involved in ribosome biogenesis and genes that evolve slowly, consistent with the hypothesis that reciprocal gene loss is more likely to occur between duplicated genes that are functionally indistinguishable. We propose a simple, unified model in which a single mechanism--passive gene loss-enabled whole--genome duplication and led to the rapid emergence of new yeast species.

Alleles↗

The willow bud galler Euura mucronata Hartig (Hymenoptera: Tenthredinidae): one polyphage or many monophages?

The nematine sawfly Euura mucronata Hartig (Hymenoptera: Tenthredinidae) induces galls in the buds of over 30 willow species across the Holarctic region. This extensive host range is surprising, since the other Euura gallers are mostly monophagous; thus, the feeding habit of E. mucronata would represent a switch from monophagy to extreme polyphagy. Previous morphological studies have divided E. mucronata into separate species, but the feeding ranges of these species are unknown, and it is even doubtful whether multiple species really exist. To study whether or not E. mucronata consists of cryptic host-associated sibling species, an allozyme study was conducted using gallers collected from six willow species occurring in northern Fennoscandia. Electrophoretic data from seven variable enzyme loci show that: (1) "E. mucronata" probably comprises at least three species with restricted host ranges, but the species may not be completely reproductively isolated from each other; (2) the pattern of host use is not explained by the phylogeny of willows; (3) the pattern of host use is not concordant with the overall chemical similarity of the hosts; and (4) simple allopatric speciation does not appear to explain the host associations. Consequently, it is possible that reasons such as differences in host phenology, habitat, or morphology, are responsible for the limits in host use in the group.

Animals↗

Microsatellite data resolve phylogeographic patterns in European grayling, Thymallus thymallus, Salmonidae.

The phylogeography of an endangered salmonid, European grayling (Thymallus thymallus), was studied based on analysis of 17 nuclear microsatellite DNA loci. In agreement with earlier mitochondrial DNA (mtDNA) studies, phylogenetic relationships of the populations suggested that northern Europe was colonized from two distinct Pleistocene refugia. Furthermore, microsatellites revealed highly supported grouping of mainland Swedish, Norwegian, Danish, German and Slovenian populations, suggesting that grayling from the northwestern and central Europe have descended from their southern conspecifics. The level of divergence between populations was substantial, even across short geographical distances. Although this was in part due to postglacial colonization patterns and contemporary barriers for gene flow, the high divergence estimates between hydrologically connected sampling locations implied efficient interpopulation reproductive isolation. Microsatellites revealed that the populations exhibited, on average, only 3.5 (+/-2.2) alleles per locus, indicating that T. thymallus has strikingly low levels of intrapopulation genetic diversity as compared with other freshwater fish species. Accordingly, as indicated by analysis of molecular variance (AMOVA), only 49.1-58.0% of the total grayling microsatellite diversity resided within populations. A latitudinal genetic diversity gradient, potentially resulting from glaciation-mediated founder events, was not evident. Alternatively, it is possible that grayling display limited dispersal behaviour/capability, leading to low long-term effective population sizes and, consequently, depauperate intrapopulation polymorphism. These findings have implications for conservation of T. thymallus. Importantly, they exemplify that microsatellites can be highly informative for intraspecific phylogeography studies dealing with substantial divergence scales.

Animals↗

Contact zones between chromosomal races of Mus musculus domesticus. 3. Molecular and chromosomal evidence of restricted gene flow between the CD race (2n = 22) and the ACR race (2n = 24).

The contact zone between the Ancarano (ACR; 2n = 24) and Cittaducale (CD; 2n = 22) races of Mus musculus domesticus was studied. We used chromosomes and mitochondrial DNA (mtDNA) sequences of the control region as genetic markers to detect introgression between races. In total, 76 mice were trapped at 17 localities. Cytogenetic analysis was performed on 73 mice. A segment of the control region (468 bp) was sequenced in 41 specimens. The two races are distributed parapatrically and the contact zone was identified inside a village (Pizzoli). No mixed population was found in the study area. The contact zone does not correspond to any geographical or ecological barrier but is located in a zone of potentially high density of mice. The sequence analysis clearly demonstrates genetic differentiation between races (1.4% of sequence divergence). Hybridization is rare. Evidence of introgression was found in two individuals in the contact zone: one individual of the ACR race carries a metacentric belonging to the CD race, while another ACR individual carries a CD-like haplotype. In these ecological conditions, the observed distribution pattern and the very low level of hybridization suggest the presence of a premating mechanism of reproductive isolation.

Animals↗

A linkage map for the hybridising toads Bombina bombina and B. variegata (Anura: Discoglossidae).

Stable hybrid zones in which ecologically divergent taxa give rise to a range of recombinants are natural laboratories in which the genetic basis of adaptation and reproductive isolation can be unraveled. One such hybrid zone is formed by the fire-bellied toads Bombina bombina and B. variegata (Anura: Discoglossidae). Adaptations to permanent and ephemeral breeding habitats, respectively, have shaped numerous phenotypic differences between the taxa. All of these are, in principle, candidates for a genetic dissection via QTL mapping. We present here a linkage map of 28 codominant and 10 dominant markers in the Bombina genome. In an F2 cross, markers that were mainly microsatellites, SSCPs or allozymes were mapped to 20 linkage groups. Among the 40 isolated CA microsatellites, we noted a preponderance of compound and frequently interleaved CA-TA repeats as well as a striking polarity at the 5' end of the repeats.

Animals↗

Molecular population divergence and sexual selection on morphology in the banded demoiselle (Calopteryx splendens).

The importance of sexual selection in population divergence is of much interest, mainly because it is thought to cause reproductive isolation and hence could lead to speciation. Sexually selected traits have been hypothesized to diverge faster between populations than other traits, presumably because of differences in the strength, mechanism or dynamics of selection. We investigated this by quantifying population divergence in eight morphological characters in 12 south Swedish populations of a sexually dimorphic damselfly, the banded demoiselle (Calopteryx splendens). The morphological characters included a secondary sexual character, the male melanized wing spot, which has an important function in both inter- and intrasexual selection. In addition, we investigated molecular population divergence, revealed by amplified fragment length polymorphism (AFLP) analysis. Molecular population divergence was highly significant among these Northern European populations (overall F(st)=0.054; pairwise population F(st)'s ranged from approximately 0 to 0.13). We found evidence for isolation-by-distance (r=0.70) for the molecular markers and a significant correlation between molecular and phenotypic population divergence (r=0.39). One interpretation is that population divergence for the AFLP loci are affected by genetic drift, but is also indirectly influenced by selection, due to linkage with loci for the phenotypic traits. Field estimates of sexual and natural selection from two of the populations revealed fairly strong sexual selection on wing spot length, indicating that this trait has the potential to rapidly diverge, provided that variation is heritable and the observed selection is chronic.

Animals↗

Genome evolution and biodiversity in teleost fish.

Teleost fish, which roughly make up half of the extant vertebrate species, exhibit an amazing level of biodiversity affecting their morphology, ecology and behaviour as well as many other aspects of their biology. This huge variability makes fish extremely attractive for the study of many biological questions, particularly of those related to evolution. New insights gained from different teleost species and sequencing projects have recently revealed several peculiar features of fish genomes that might have played a role in fish evolution and speciation. There is now substantial evidence that a round of tetraploidization/rediploidization has taken place during the early evolution of the ray-finned fish lineage, and that hundreds of duplicate pairs generated by this event have been maintained over hundreds of millions of years of evolution. Differential loss or subfunction partitioning of such gene duplicates might have been involved in the generation of fish variability. In contrast to mammalian genomes, teleost genomes also contain multiple families of active transposable elements, which might have played a role in speciation by affecting hybrid sterility and viability. Finally, the amazing diversity of sex determination systems and the plasticity of sex chromosomes observed in teleost might have been involved in both pre- and postmating reproductive isolation. Comparison of data generated by current and future genome projects as well as complementary studies in other species will allow one to approach the molecular and evolutionary mechanisms underlying genome diversity in fish, and will certainly significantly contribute to our understanding of gene evolution and function in humans and other vertebrates.

Animals↗

Culex pipiens in London Underground tunnels: differentiation between surface and subterranean populations.

Genetic variation was quantified between surface-dwelling populations of Culex pipiens and the so-called molestus form found in the London Underground (the Underground) railway system. The molestus form is a commercially important biting nuisance and in the southern part of its range is also a disease vector. The surface and subterranean populations were genetically distinct, with no evidence of gene flow between closely adjacent populations of the different forms, whereas there was little differentiation between the different populations of each form. The substantially reduced heterozygosity in the Underground populations and the allelic composition suggest that colonization of the Underground has occurred once or very few times. Breeding experiments show compatibility between the Underground populations but not with those breeding above ground. There is evidence of greater gene flow and a mixing of molestus and pipiens traits in the south of the species range. This paper considers the processes that may allow establishment of reproductive isolation in the north of the species range but not in the south.

Adaptation, Physiological↗