Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation

Chromosomal rearrangements can promote reproductive isolation by reducing recombination along a large section of the genome. We model the effects of the genetic barrier to gene flow caused by a chromosomal rearrangement on the rate of accumulation of postzygotic isolation genes in parapatry. We find that, if reproductive isolation is produced by the accumulation in parapatry of sets of alleles compatible within but incompatible across species, chromosomal rearrangements are far more likely to favor it than classical genetic barriers without chromosomal changes. New evidence of the role of chromosomal rearrangements in parapatric speciation suggests that postzygotic isolation is often due to the accumulation of such incompatibilities. The model makes testable qualitative predictions about the genetic signature of speciation.     

Chromosomal rearrangements directly cause underdominant F1 pollen sterility in Mimulus lewisii–Mimulus cardinalis hybrids

Chromosomal rearrangements can contribute to the evolution of postzygotic reproductive isolation directly, by disrupting meiosis in F₁ hybrids, or indirectly, by suppressing recombination among genic incompatibilities. Because direct effects of rearrangements on fertility imply fitness costs during their spread, understanding the mechanism of F₁ hybrid sterility is integral to reconstructing the role(s) of rearrangements in speciation. In hybrids between monkeyflowers Mimulus cardinalis and Mimulus lewisii, rearrangements contain all quantitative trait loci (QTLs) for both premating barriers and pollen sterility, suggesting that they may have facilitated speciation in this model system. We used artificial chromosome doubling and comparative mapping to test whether heterozygous rearrangements directly cause underdominant male sterility in M. lewisii–M. cardinalis hybrids. Consistent with a direct chromosomal basis for hybrid sterility, synthetic tetraploid F₁s showed highly restored fertility (83.4% pollen fertility) relative to diploids F₁s (36.0%). Additional mapping with Mimulus parishii–M. cardinalis and M. parishii–M. lewisii hybrids demonstrated that underdominant male sterility is caused by one M. lewisii specific and one M. cardinalis specific reciprocal translocation, but that inversions had no direct effects on fertility. We discuss the importance of translocations as causes of reproductive isolation, and consider models for how underdominant rearrangements spread and fix despite intrinsic fitness costs.     

Chromosome evolution in eukaryotes: a multi-kingdom perspective

In eukaryotes, chromosomal rearrangements, such as inversions, translocations and duplications, are common and range from part of a gene to hundreds of genes. Lineage-specific patterns are also seen: translocations are rare in dipteran flies, and angiosperm genomes seem prone to polyploidization. In most eukaryotes, there is a strong association between rearrangement breakpoints and repeat sequences. Current data suggest that some repeats promoted rearrangements via non-allelic homologous recombination, for others the association might not be causal but reflects the instability of particular genomic regions. Rearrangement polymorphisms in eukaryotes are correlated with phenotypic differences, so are thought to confer varying fitness in different habitats. Some seem to be under positive selection because they either trap favorable allele combinations together or alter the expression of nearby genes. There is little evidence that chromosomal rearrangements cause speciation, but they probably intensify reproductive isolation between species that have formed by another route.     

Restriction endonuclease and molecular analyses of three rat genomes with special reference to chromosome rearrangement and speciation problems

When differences are found between related species of organisms, it is often assumed that the differences themselves are causal factors either in speciation itself or in processes related to speciation. Two recent proposals on the functions of satellite DNA (Hatch et al., 1976 and Fry and Salser, 1977) are that (a) large amounts of satellite DNA are important in facilitating chromosome rearrangements and hence cytogenetic evolution, and (b) satellite DNA differences between homologous chromosomes lead to pairing difficulties and are important in generating infertility barriers and hence speciation. If these proposals were to have some generality, one could expect organisms with very low amounts of highly repeated DNA to exhibit few chromosome rearrangements and to be evolutionarily conservative in a cyto-genetic sense. — We have chosen two very closely related species of rat which are phenotypically almost indistinguishable and which have undergone massive genome reorganization. They differ by 11 major centric rearrangements (2n=32, 2n=50). We have characterised their genomes by restriction endonuclease digestions, thermal denaturations, analytical ultracentrifugations and reassociation techniques, and have found that they have virtually no highly repeated DNA. Thus the 11 major chromosomal rearrangements have been fixed in present day genomes with hardly any highly repeated DNA, centric or otherwise. — It appears therefore that a large amount of highly repeated DNA is not obligatory for the formation and fixation of chromosome rearrangements. In addition, the existing literature reveals that one can find almost any situation at all, from species groups with high amounts of satellite DNA and no gross chromosomal rearrangements, to ones such as those described here, with tiny amounts of highly repeated DNA and massive chromosomal reorganisation. Since direct experimental data indicates that satellite DNA differences per se between homologous chromosomes do not cause infertility, speculations concerning modes of speciation based on satellite DNA differences between otherwise homologous chromosomes would appear to be ill founded.     

Recent radiation in West African Taterillus (Rodentia, Gerbillinae): the concerted role of chromosome and climatic changes

West African gerbils of the genus Taterillus constitute a complex of seven sibling species distributed from sudano-guinean to saharo-sahelian regions. They display radically rearranged karyotypes despite low genic divergence and a very recent differentiation, that is, within the last 0.4 Myr for the six most derived species. We here provide a comparison of the seven specific karyotypes and perform a cladistic analysis using chromosomal rearrangements character states. When a posteriori polarized mutations were mapped onto the phylogenetic tree, 38 rearrangements were identified as fixed during the evolution of these rodents. This makes Taterillus one of the most striking examples of accelerated chromosomal evolution within placental mammals. Taking into account the types of chromosomal changes involved, divergence times between lineages, genetic distances, as well as reassessed geographic distributions, we suggest that (1) speciation in West African Taterillus was driven by chromosomal changes, and (2) the paleoclimatic oscillations of the Sahara desert have played a major role in their evolution. In particular, elevated plasticity of the Taterillus genome, as suggested by the patterns observed for some repetitive elements, would have led to a higher probability of mutation. We hypothesize that the process underpinning cladogenesis most probably involved highly underdominant genomic rearrangements that were fixed following pronounced populational bottlenecks resulting from drastic climatic and subsequent environmental changes. Major African rivers formed significant barriers to dispersal, limiting expansion during the more moist and so favorable periods. This scenario would explain the current parapatric species distributions and their relationship to the West African hydrographic features.     

Chromosomal rearrangements are associated with higher rates of molecular evolution in mammals

Evolutionary rates are not uniformly distributed across the genome. Knowledge about the biological causes of this observation is still incomplete, but its exploration has provided valuable insight into the genomical, historical and demographical variables that influence rates of genetic divergence. Recent studies suggest a possible association between chromosomal rearrangements and regions of greater divergence, but evidence is limited and contradictory. Here, we test the hypothesis of a relationship between chromosomal rearrangements and higher rates of molecular evolution by studying the genomic distribution of divergence between 12,000 human-mouse orthologous genes. Our results clearly show that genes located in genomic regions that have been highly rearranged between the two species present higher rates of synonymous (0.7686 vs. 0.7076) and non-synonymous substitution (0.1014 vs. 0.0871), and that synonymous substitution rates are higher in genes close to the breakpoints of individual rearrangements. The many potential causes of such striking are discussed, particularly in the light of speciation models suggesting that chromosomal rearrangements may have contributed to some of the speciation processes along the human and mouse lineages. Still, there are other possible causes and further research is needed to properly explore them.     

Multiple chromosomal rearrangements in a hybrid zone between Littorina saxatilis ecotypes

Both classical and recent studies suggest that chromosomal inversion polymorphisms are important in adaptation and speciation. However, biases in discovery and reporting of inversions make it difficult to assess their prevalence and biological importance. Here, we use an approach based on linkage disequilibrium among markers genotyped for samples collected across a transect between contrasting habitats to detect chromosomal rearrangements de novo. We report 17 polymorphic rearrangements in a single locality for the coastal marine snail, Littorina saxatilis. Patterns of diversity in the field and of recombination in controlled crosses provide strong evidence that at least the majority of these rearrangements are inversions. Most show clinal changes in frequency between habitats, suggestive of divergent selection, but only one appears to be fixed for different arrangements in the two habitats. Consistent with widespread evidence for balancing selection on inversion polymorphisms, we argue that a combination of heterosis and divergent selection can explain the observed patterns and should be considered in other systems spanning environmental gradients.     

Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes

Chromosomal change is one of the more hotly debated potential mechanisms of speciation. It has long been argued over whether--and to what degree--changes in chromosome structure contribute to reproductive isolation and, ultimately, speciation. In this review we do not aim to completely analyze accumulated data about chromosomal speciation but wish to draw attention to several critical points of speciation-related chromosomal change, namely: (a) interrelations between chromosomal rearrangements and repetitive DNA fraction; (b) mobility of ribosomal DNA clusters; and (c) rDNA and transposable elements as perpetual generators of genome instability.     

On the association between chromosomal rearrangements and genic evolution in humans and chimpanzees

Background  

The role that chromosomal rearrangements might have played in the speciation processes that have separated the lineages of humans and chimpanzees has recently come into the spotlight. To date, however, results are contradictory. Here we revisit this issue by making use of the available human and chimpanzee genome sequence to study the relationship between chromosomal rearrangements and rates of DNA sequence evolution.     

Chromosomal variation segregates within incipient species and correlates with reproductive isolation

Reproductive isolation is a critical step in the process of speciation. Among the most important factors driving reproductive isolation are genetic incompatibilities. Whether these incompatibilities are already present before extrinsic factors prevent gene flow between incipient species remains largely unresolved in natural systems. This question is particularly challenging because it requires that we catch speciating populations in the act before they reach the full‐fledged species status. We measured the extent of intrinsic postzygotic isolation within and between phenotypically and genetically divergent lineages of the wild yeast Saccharomyces paradoxus that have partially overlapping geographical distributions. We find that hybrid viability between lineages progressively decreases with genetic divergence. A large proportion of postzygotic inviability within lineages is associated with chromosomal rearrangements, suggesting that chromosomal differences substantially contribute to the early steps of reproductive isolation within lineages before reaching fixation. Our observations show that polymorphic intrinsic factors may segregate within incipient species before they contribute to their full reproductive isolation and highlight the role of chromosomal rearrangements in speciation. We propose different hypotheses based on adaptation, biogeographical events and life history evolution that could explain these observations.     

The role of deleterious mutations in allopatric speciation

Allopatric speciation is often assumed to occur as a consequence of adaptive divergence between two isolated populations. However, there are some scenarios in which reproductive isolation can be favored due to accumulated unconditionally deleterious mutations. If deleterious mutations have synergistic epistatic effects, it is shown here that the average fitness of recombinants between two parental lines with a given number of fixed mutations is lower than that of the parents in both the F1 and F2 generations. If individual mutations are only slightly deleterious, then they will tend to fixation at a high enough rate to cause lower hybrid fitness. If the fitness effects of mutation give rise to antagonistic epistasis, the hybrids tend to have a higher average fitness than the parental lines, suggesting a possible scenario for the origin of hybrid vigor. The other model of deleterious mutations investigated is the accumulation of knockout mutants in a duplicated gene family. While neutral in the parental lines, upon contact the F1 and later generations have a significant probability of carrying double knockouts. Under this scenario, selection may also favor reproductive isolation between the two lines. Even when the selection coefficients generated are too low to drive speciation, epistatic interactions between deleterious mutations offer a possible explanation for both outbreeding depression and hybrid vigor.     

Chromosomal rearrangements and the genomic distribution of gene-expression divergence in humans and chimpanzees

The genomic DNA sequences of humans and chimpanzees differ by only 1.24%. Recently, however, substantial differences in gene-expression patterns between the two species have been revealed. In this article, we investigate the genomic distribution of such differences. Besides confirming previous findings about the evolution of sex chromosomes and duplications, we show that chromosomal rearrangements are associated with increased gene-expression differences in the brain and that rearrangements can have both direct and indirect effects on the expression of linked genes. In addition, our results are consistent with a role for some rearrangements in the original speciation events that separated the human and chimpanzee lineages.     

Episodic chromosomal evolution in Planipapillus (Onychophora: Peripatopsidae): a phylogenetic approach to evolutionary dynamics and speciation

Planipapillus, a clade of onychophorans from southeastern Australia, exhibits substantial chromosomal variation. In the context of a robust phylogeny based on nuclear and mitochondrial sequence data, we evaluate models of chromosomal evolution and speciation that differ in the roles assigned to selection, mutation, and drift. Permutation tests suggest that all chromosome rearrangements in the clade have been centric fusions and, on the basis of parsimony and maximum-likelihood methods with independent estimates of branch lengths, we conclude that at least 31 centric fusions have been fixed in Planipapillus. A likelihood-ratio test approach, which is independent of our point estimates of ancestral states, rejects an evolutionary model in which the mutation rate is constant and centric fusions are effectively neutral. In contrast to the nucleotide sequence data, which are consistent with neutrality and rate constancy, centric fusions in Planipapillus are underdominant, spontaneous fusion rates vary among lineages, or both. We predict an inverse relationship between rates of chromosomal evolution and historical population size. Chromosomal evolution may play a role in speciation in Planipapillus, both by interactions between centric fusions with monobrachial homology and by the accumulation of multiple weakly underdominant fusions.     

Genetic instability and rapid speciation: are they coupled?

Models of rapid speciation by fixation of underdominant chromosomal rearrangements are constrained by multiple conditions on population structure and chromosomal performance. Realistic population conditions impose long periods of time to fixation or reproductive isolation, even under a model of accumulation of successive advantageous slightly underdominant rearrangements. However, when increased mutation rates are considered, fixation time is significantly reduced. Evidence is presented of high rates of chromosomal rearrangement production under genomic stress, such as in inbred and interspecific crosses. These episodes of high instability are most probably the result of mobile element transpositions, since transposition is also increased under genomic stress. Nonetheless, the evolutionary value of mobile elements to speed up speciation will be only significant if their mutagenic potential is activated in concert with population scenarios favorable to speciation events. Although this coupling needs to be demonstrated, many models of rapid speciation are carried out under population conditions favoring inbreeding and/or hybridization.     

Karyotypic diversity and speciation in Agrodiaetus butterflies

That chromosomal rearrangements may play an important role in maintaining postzygotic isolation between well-established species is part of the standard theory of speciation. However, little evidence exists on the role of karyotypic change in speciation itself--in the establishment of reproductive barriers between previously interbreeding populations. The large genus Agrodiaetus (Lepidoptera: Lycaenidae) provides a model system to study this question. Agrodiaetus butterflies exhibit unusual interspecific diversity in chromosome number, from n= 10 to n= 134; in contrast, the majority of lycaenid butterflies have n= 23/24. We analyzed the evolution of karyotypic diversity by mapping chromosome numbers on a thoroughly sampled mitochondrial phylogeny of the genus. Karyotypic differences accumulate gradually between allopatric sister taxa, but more rapidly between sympatric sister taxa. Overall, sympatric sister taxa have a higher average karyotypic diversity than allopatric sister taxa. Differential fusion of diverged populations may account for this pattern because the degree of karyotypic difference acquired between allopatric populations may determine whether they will persist as nascent biological species in secondary sympatry. This study therefore finds evidence of a direct role for chromosomal rearrangements in the final stages of animal speciation. Rapid karyotypic diversification is likely to have contributed to the explosive speciation rate observed in Agrodiaetus, 1.6 species per million years.     

Variance and variability,uncovering an underappreciated component of reproductive isolation

Estimating the fitness of line crosses has been a key element in studies of inbreeding depression, hybridization, and speciation. Fitness values are typically compared using differences in the arithmetic mean of a fitness component between types of crosses. One aspect of fitness that is often overlooked is variance in offspring fitness over time. In the majority of studies, ignoring this aspect of fitness is unavoidable because it is impossible to estimate variance in offspring fitness over long time periods. Here, I describe a method of estimating variance in offspring fitness by substituting spatial variation for temporal variation and provide an empirical example. The method is based on Levene's test of homogeneity of variances. It is implemented by quantifying differences in residual variation among cross types. In a previous study, I performed crosses between populations of the annual plant Diodia teres and quantified hybrid fitness. In this study, another component of isolation and heterosis was revealed when considering variance in offspring fitness. When taking into account variance in offspring fitness using geometric mean fitness as the measure of performance, hybrids between populations from different habitats showed less heterosis than when calculating fitness based on arithmetic mean. This study demonstrates that variance in offspring fitness can be an important aspect of fitness that should be measured more frequently.     

Genetic analysis of a chromosomal hybrid zone in the Australian morabine grasshoppers (Vandiemenella, viatica species group)

Whether chromosomal rearrangements promote speciation by providing barriers to gene exchange between populations is one of the long-standing debates in evolutionary biology. This question can be addressed by studying patterns of gene flow and selection in hybrid zones between chromosomally diverse taxa. Here we present results of the first study of the genetic structure of a hybrid zone between chromosomal races of morabine grasshoppers Vandiemenella viatica , P24(XY) and viatica 17, on Kangaroo Island, Australia. Chromosomal and 11 nuclear markers revealed a narrow hybrid zone with strong linkage disequilibrium and heterozygote deficits, most likely maintained by a balance between dispersal and selection. Widths and positions of clines for these markers are concordant and coincident, suggesting that selection is unlikely to be concentrated on a few chromosomes. In contrast, a mitochondrial marker showed a significantly wider cline with centre offset toward the P24(XY) side. We argue that the discordance between the mitochondrial and nuclear/chromosomal clines and overall asymmetry of the clines suggest a secondary origin of the contact zone and potential movement of the zone after contact. Genome-wide scans using many genetic markers and chromosomal mapping of these markers are needed to investigate whether chromosomal differences directly reduce gene flow after secondary contact.     

Speciation in the apple maggot fly: a blend of vintages?

The importance of speciation without the complete geographical separation of diverging populations (sympatric speciation) has become increasingly accepted. One of the textbook examples of recent speciation in sympatry is the apple maggot fly Rhagoletis pomonella, in which genetically differentiated host races feed on either hawthorn or apple. Three recent articles by Feder and collaborators show that the history of these host races is more complicated than was previously realized. Genes that differentiate races of flies that feed on either apple or hawthorn are located in chromosomal rearrangements. This variation forms a latitudinal cline that must have been established long before apples were available as hosts. Furthermore, there is also new evidence for the very recent evolution of a derived preference for volatile chemicals that are typical of apple fruits among apple-feeding flies. These results show that adaptation to apple populations has involved both the sorting of ancestral adaptive variation and the selection of novel mutations.     

Polytene chromosome relationships of five species of the Anopheles dirus complex in Thailand.

Photographic maps and rearrangements of each salivary gland polytene chromosome arm of Anopheles nemophilous (species F) and of An. dirus species A, B, C, and D of the Dirus group from natural populations in Thailand are presented. Structural conformation of heterokaryotypes and comparison of chromosome banding sequences reveal 10 paracentric inversions. The data on fixed inversion of 3Rb and inversion polymorphism of the X chromosome shared by these species were used to construct a phylogeny of the five members of the An. dirus complex, thereby outlining their patterns of speciation through chromosomal rearrangements.     

A genetic interpretation of ecologically dependent isolation

Hybrids may suffer a reduced fitness both because they fall between ecological niches (ecologically dependent isolation) and as a result of intrinsic genetic incompatibilities between the parental genomes (ecologically independent isolation). Whereas genetic incompatibilities are common to all theories of speciation, ecologically dependent isolation is a unique prediction of the ecological model of speciation. This prediction can be tested using reciprocal transplants in which the fitness of various genotypes is evaluated in both parental habitats. Here we expand a quantitative genetic model of Lynch (1991) to include two parental environments. We ask whether a sufficient experimental design exists for detecting ecologically dependent isolation. Analysis of the model reveals that by using both backcrosses in both parental environments, environment-specific additive genetic effects can be estimated while correcting for any intrinsic genetic isolation. Environment-specific dominance effects can also be estimated by including the F1 and F2 in the reciprocal transplant. In contrast, a reciprocal transplant comparing only F1s or F2s to the parental species cannot separate ecologically dependent from intrinsic genetic isolation. Thus, a reduced fitness of F1 or F2 hybrids relative to the parental species is not sufficient to demonstrate ecological speciation. The model highlights the importance of determining the contribution of genetic and ecological mechanisms to hybrid fitness if inferences concerning speciation mechanisms are to be made.