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The evolution of hybrid infertility: perpetual coevolution between gender-specific and sexually antagonistic genes.

A new hypothesis is proposed for the rapid evolution of postzygotic reproductive isolation via hybrid infertility. The hypothesis is motivated by two lines of experimental research from Drosophila melanogaster that demonstrate that sexually antagonistic fitness variation is abundant and that epistatic fitness variation on the Y chromosome is common. The hypothesis states that the expression of sexually antagonistic genes leads to a 'gender-load' in each sex. In response, gender-limited reproductive genes are selected to ameliorate, through pleiotropy, the expression of sexually antagonistic genes. Chronic coevolution between gender-limited genes and gender-unlimited sexually antagonistic genes causes rapid divergence of reproductive proteins among allopatric populations, ultimately leading to hybrid infertility.

Animals↗

Genetic distance and species formation in evolving populations.

We compare the behavior of the genetic distance between individuals in evolving populations for three stochastic models. In the first model reproduction is asexual and the distribution of genetic distances reflects the genealogical tree of the population. This distribution fluctuates greatly in time, even for very large populations. In the second model reproduction is sexual with random mating allowed between any pair of individuals. In this case, the population becomes homogeneous and the genetic distance between pairs of individuals has small fluctuations which vanish in the limit of an infinitely large population. In the third model reproduction is still sexual but instead of random mating, mating only occurs between individuals which are genetically similar to each other. In that case, the population splits spontaneously into species which are in reproductive isolation from one another and one observes a steady state with a continual appearance and extinction of species in the population. We discuss this model in relation to the biological theory of speciation and isolating mechanisms. We also point out similarities between these three models of evolving populations and the theory of disordered systems in physics.

Biological Evolution↗

LETHAL ALLELES IN MUS MUSCULUS: LOCAL DISTRIBUTION AND EVIDENCE FOR ISOLATION OF DEMES.

In the vicinity of Calgary, Alberta, 20.5 percent of wild house mice tested were found to be heterozygous for the lethal allele designated t(w5), and an additional 3.4 percent were heterozygous for one or more alleles not belonging to the t(w5) group. The distribution patterns of wild-type and lethal alleles within and between clusters of small demes supports the postulate that random drift plays a significant role in the evolution of these populations. Distribution patterns also suggest that the demes are reproductively isolated to a greater degree than has been generally assumed.

Alleles↗

Phylogeography and speciation of colour morphs in the colonial ascidian Pseudodistoma crucigaster.

Variation in pigmentation is common in marine invertebrates, although few studies have shown the existence of genetic differentiation of chromatic forms in these organisms. We studied the genetic structure of a colonial ascidian with populations of different colour morphs in the northwestern Mediterranean. A fragment of the c oxidase subunit 1 (COI) mitochondrial gene was sequenced in seven populations of Pseudodistoma crucigaster belonging to three different colour morphs (orange, yellow and grey). Maximum likelihood analyses showed two well-supported clades separating the orange morph from the yellow-grey morphotypes. Genetic divergence between these clades was 2.12%, and gamma(ST) values between populations of the two clades were high (average 0.936), pointing to genetic isolation. Nested clade and coalescence analyses suggest that a past fragmentation event may explain the phylogeographical origin of these two clades. Non-neutral mtDNA evolution is observed in our data when comparing the two clades, showing a significant excess of nonsynonymous polymorphism within the yellow-grey morphotype using the McDonald-Kreitman test, which is interpreted as further support of reproductive isolation. We conclude that the two clades might represent separate species. We compare the population genetic differentiation found with that estimated for other colonial and solitary ascidian species, and relate it to larval dispersal capabilities and other life-history traits.

Animals↗

Endogamy and variation in blood pressure levels in Croatian island isolates.

Blood pressure variation was investigated among populations inhabiting islands and peninsula of Middle Dalmatia, Croatia. The number of previous anthropological studies pointed to isolation and different genetic population structure in this environmentally fairly homogeneous area. Variation in blood pressure (systolic and diastolic) among the populations of the islands of Brac, Hvar, Korcula, and the Peljesac peninsula was assessed at three levels involving village populations, regional (western and eastern) populations and the entire island populations. The blood pressure data were collected from 3834 adult individuals inhabiting 37 rural communities and were adjusted for age and body mass index. Variation in blood pressure levels existed among regions and villages. Due to the history of differential settlement, small village sizes and high levels of reproductive isolation, the observed blood pressure variation could be attributed to founder effect, genetic drift and inbreeding. The involvement of genetic factors was tested by relating blood pressure variation among villages to degree of isolation among them. Blood pressure means and proportions of hypertensives increased with endogamy levels in males. In females, this effect could not be observed. However, in both sexes the highest proportions of hypertensives (more than 40%) were found in villages that are most reproductively closed (endogamy greater than 80%). These populations are considered particularly promising for further genetic epidemiological research.

Anthropology, Cultural↗

A rapidly evolving homeobox at the site of a hybrid sterility gene.

The homeodomain is a DNA binding motif that is usually conserved among diverse taxa. Rapidly evolving homeodomains are thus of interest because their divergence may be associated with speciation. The exact site of the Odysseus (Ods) locus of hybrid male sterility in Drosophila contains such a homeobox gene. In the past half million years, this homeodomain has experienced more amino acid substitutions than it did in the preceding 700 million years; during this period, it has also evolved faster than other parts of the protein or even the introns. Such rapid sequence divergence is driven by positive selection and may contribute to reproductive isolation.

Amino Acid Sequence↗

Natural selection and parallel speciation in sympatric sticklebacks.

Natural selection plays a fundamental role in most theories of speciation, but empirical evidence from the wild has been lacking. Here the post-Pleistocene radiation of threespine sticklebacks was used to infer natural selection in the origin of species. Populations of sticklebacks that evolved under different ecological conditions show strong reproductive isolation, whereas populations that evolved independently under similar ecological conditions lack isolation. Speciation has proceeded in this adaptive radiation in a repeatable fashion, ultimately as a consequence of adaptation to alternative environments.

Adaptation, Physiological↗

Evidence for subdivision of the root-endophyte Phialocephala fortinii into cryptic species and recombination within species.

The genetic structure of the root-endophyte Phialocephala fortinii was analyzed in three study sites using 11 single-copy RFLP probes. A total of 541 strains isolated from surface-sterilized, fine roots (diameter 0.5-3 mm) of Norway spruce (Picea abies) were examined. The average gene diversity (H) was high in all three study sites. Cluster analysis showed that up to four well-separated clusters of multi-locus haplotypes were present within the sites. Significant population subdivision was detected among these clusters, suggesting that groups of multi-locus haplotypes were reproductively isolated and that P. fortinii is a species complex composed of several cryptic species. This hypothesis was supported by ISSR-PCR which showed clusters consistent with those of the multi-locus haplotypes identified by RFLP analysis. In contrast, ITS sequence analysis did not allow to separate the species as clearly. The index of association (IA) did not deviate significantly from zero within any cryptic species, suggesting that recombination occurs within these species. Cryptic species occurred sympatrically. Thalli of two cryptic species were detected in the same 5-mm-long root segment in one instance. No significant differentiation was observed among populations of the same cryptic species in forest stands located approximately 5 km from each other. This finding is consistent with significant gene flow over this spatial scale. In addition, several isolates with both identical multi-locus haplotype and identical ISSR fingerprint were found at each study site indicating genotype flow or a recent common history between study sites.

Ascomycota↗

Speciation and biogeography of the Caloglossa leprieurii complex (Delesseriaceae, Rhodophyta).

Studies on the morphology, reproductive compatibility, life cycle and molecular phylogeny of the euryhaline red alga Caloglossa provide insights into the speciation events and biogeographic patterns. The C. leprieurii complex is separated into three morphotypes based on the number of cell rows at nodes and the blade width. The three morphotypes are reproductively incompatible with each other, and furthermore many mating groups are recognized within the morphotypes. Incomplete reproductive isolation is occasionally seen between geographically distant mating groups, whereas no sexual compatibility occurs between sympatrically or parapatrically distributed mating groups. In the molecular phylogenetic analyses, the C. leprieurii complex is resolved as two clusters that phenotypically correspond to the single and multiple cell row types, respectively. The strains belonging to the same mating group are closely related to each other, without exception, while the mating groups showing incomplete reproductive reactions do not always make a clade. The genetic distance is generally not correlative to the geographic distance, and this is also suggested by the morphological data and crossability. These results indicate that allopatric speciation has frequently occurred in this species complex, although there is some evidence of long-distance dispersal.

Brazil↗

The discovery of three genetic races of the dwarf mistletoe Arceuthobium americanum (Viscaceae) provides insight into the evolution of parasitic angiosperms.

A population genetic approach was used to explore the evolutionary biology of the parasitic angiosperm Arceuthobium americanum Nutt. ex Engelm. (Viscaceae). Arceuthobium americanum infects three principal hosts and has the most extensive geographical range of any North American dwarf mistletoe. Based on the lack of apparent morphological and phenological differences between populations of A. americanum, past researchers have found no evidence for recognizing infraspecific taxa. In this study, molecular analysis using amplified fragment length polymorphism (AFLP) analysis indicated that A. americanum is divided into three distinct genetic races, each associated with a different host taxon in regions of allopatry: (i) Pinus banksiana in western Canada; (ii) Pinus contorta var. murrayana in the Sierra Nevada and Cascade Mountain ranges in the western US; and (iii) Pinus contorta var. latifolia in the western US and Canada. These observations suggest that host identity, geographical isolation and environmental factors have contributed to race formation in A. americanum. The lack of fine-scale patterning within each of the A. americanum races is attributed to random dispersal of seeds over long distances by animal vectors. Historical factors such as glaciations and founder events have also influenced structuring and genetic diversity in A. americanum populations. Given sufficient time, it is possible that these races will become reproductively isolated and undergo speciation.

Biological Evolution↗

Hybridization between Aedes simpsoni and Aedes woodi with observations on the genetic basis of morphological differences.

The public health importance of the genus Aedes makes it imperative that a better understanding of the genetic differences and isolating barriers between the species be developed. Aedes simpsoni and Aedes woodi from near Dar es Salaam, Tanzania, were used in this investigation. Analysis of F(1), F(2), and backcross progeny obtained from forced matings indicates that single factors form the genetic basis of some of the differences between the two species. There is evidence that Ae. simpsoni and Ae. woodi are separated by both premating and postmating reproductive isolating mechanisms.

Aedes↗

Sequence analysis of open reading frames (ORFs) 2 to 4 of a U.S. isolate of porcine reproductive and respiratory syndrome virus.

The sequence of ORFs 2 to 4 of a U.S. isolate of porcine reproductive and respiratory syndrome virus (PRRSV), ATCC VR2385, was determined by analysis of a cDNA lambda library. The cDNA clones containing PRRSV specific sequences were selected using a VR2385 ORF 4 specific PCR probe and sequenced. The ORFs 2, 3 and 4 overlapped each other and encoded polypeptides with predicted M(r) of 29.5 kDa (ORF 2), 28.7 kDa (ORF 3) and 19.5 kDa (ORF 4), respectively. No overlap was found between ORFs 4 and 5, and instead there was a 10 bp sequence which separated these two ORFs. The nucleic acid homology with corresponding ORFs of the European PRRSV isolate Lelystad virus (LV) was 65% for ORF 2, 64% for ORF 3 and 66% for ORF 4. Comparison of the ORF 4 sequences of VR2385 with that of another U.S. isolate MN-1b revealed only 86% amino acid sequence homology and the presence of deletions in the ORF 4 of MN-1b. Our results further strengthen the observation that there is sequence variation between US and European PRRSV isolates.

Amino Acid Sequence↗

Homoploid hybrid speciation in an extreme habitat.

According to theory, homoploid hybrid speciation, which is hybrid speciation without a change in chromosome number, is facilitated by adaptation to a novel or extreme habitat. Using molecular and ecological data, we found that the alpine-adapted butterflies in the genus Lycaeides are the product of hybrid speciation. The alpine populations possess a mosaic genome derived from both L. melissa and L. idas and are differentiated from and younger than their putative parental species. As predicted, adaptive traits may allow for persistence in the environmentally extreme alpine habitat and reproductively isolate these populations from their parental species.

Adaptation, Physiological↗

Incipient speciation by sexual isolation in Drosophila: concurrent evolution at multiple loci.

Drosophila melanogaster from Zimbabwe and nearby regions shows strong but asymmetric sexual isolation from its cosmopolitan counterparts. By creating stable chromosome-substitution lines, earlier studies were able to show that the two major autosomes have very large effects on both male mating success and female mating preference. In this study, we genetically dissect this sexual isolation by recombination analysis between a whole-chromosome substitution line (which carries a Zimbabwe-derived third chromosome) and a strain with seven visible markers on that chromosome. Four loci are responsible for male mating success and three others are found to control female mating preference. Because male and female traits are not closely linked, their strong association among isofemale lines is most likely a reflection of sexual selection in nature. The results suggest that a large number of behavioral loci may evolve concurrently in the incipient stage of speciation before other aspects of reproductive isolation (such as hybrid sterility) have become evident. The results shed light on the population genetic processes underlying the formation of nascent species, as well as modes of speciation.

Animals↗

Postzygotic incompatibilities between the pupfishes, Cyprinodon elegans and Cyprinodon variegatus: hybrid male sterility and sex ratio bias.

I examined the intrinsic postzygotic incompatibilities between two pupfishes, Cyprinodon elegans and Cyprinodon variegatus. Laboratory hybridization experiments revealed evidence of strong postzygotic isolation. Male hybrids have very low fertility, and the survival of backcrosses into C. elegans was substantially reduced. In addition, several crosses produced female-biased sex ratios. Crosses involving C. elegans females and C. variegatus males produced only females, and in backcrosses involving hybrid females and C. elegans males, males made up approximately 25% of the offspring. All other crosses produced approximately 50% males. These sex ratios could be explained by genetic incompatibilities that occur, at least in part, on sex chromosomes. Thus, these results provide strong albeit indirect evidence that pupfish have XY chromosomal sex determination. The results of this study provide insight on the evolution of reproductive isolating mechanisms, particularly the role of Haldane's rule and the 'faster-male' theory in taxa lacking well-differentiated sex chromosomes.

Animals↗

Geographic variation of genetic and behavioral traits in northern and southern tüngara frogs.

We use a combination of microsatellite marker analysis and mate-choice behavior experiments to assess patterns of reproductive isolation of the túngara frog Physalaemus pustulosus along a 550-km transect of 25 populations in Costa Rica and Panama. Earlier studies using allozymes and mitochondrial DNA defined two genetic groups of túngara frogs, one ranging from Mexico to northern Costa Rica (northern group), the second ranging from Panama to northern South America (southern group). Our more fine-scale survey also shows that the northern and southern túngara frogs are genetically different and geographically separated by a gap in the distribution in central Pacific Costa Rica. Genetic differences among populations are highly correlated with geographic distances. Temporal call parameters differed among populations as well as between genetic groups. Differences in calls were explained better by geographic distance than by genetic distance. Phonotaxis experiments showed that females preferred calls of males from their own populations over calls of males from other populations in about two-thirds to three-fourths of the contrasts tested. In mating experiments, females and males from the same group and females from the north with males from the south produced nests and tadpoles. In contrast, females from the south did not produce nests or tadpoles with males from the north. Thus, northern and southern túngara frogs have diverged both genetically and bioacoustically. There is evidence for some prezygotic isolation due to differences in mate recognition and fertilization success, but such isolation is hardly complete. Our results support the general observation that significant differences in sexual signals are often not correlated with strong genetic differentiation.

Animals↗

A locus for female discrimination behavior causing sexual isolation in Drosophila.

The genetic basis of sexual isolation that contributes to speciation is one of the unsolved questions in evolutionary biology. Drosophila ananassae and Drosophila pallidosa are closely related, and postmating isolation has not developed between them. However, females of both species discriminate their mating partners, and this discrimination contributes to strong sexual isolation between them. By using surgical treatments, we demonstrate that male courtship songs play a dominant role in female mate discrimination. The absence of the song of D. pallidosa dramatically increased interspecies mating with D. ananassae females but reduced intraspecies mating with D. pallidosa females. Furthermore, genetic analysis and chromosomal introgression by repeated backcrosses to D. pallidosa males identified possible loci that control female discrimination in each species. These loci were mapped on distinct positions near the Delta locus on the middle of the left arm of the second chromosome. Because the mate discrimination we studied is well developed and is the only known mechanism that prevents gene flow between them, these loci may have played crucial roles in the evolution of reproductive isolation, and therefore, in the speciation process between these two species.

Animals↗

The evolutionary genetics of speciation.

The last decade has brought renewed interest in the genetics of speciation, yielding a number of new models and empirical results. Defining speciation as 'the origin of reproductive isolation between two taxa', we review recent theoretical studies and relevant data, emphasizing the regular patterns seen among genetic analyses. Finally, we point out some important and tractable questions about speciation that have been neglected.

Animals↗