Unprecedented chromosomal diversity and behaviour modify linkage patterns and speciation potential: structural heterozygosity in an Australian spider

The Huntsman spider Delena cancerides shows an extraordinary level of chromosomal diversity and meiotic complexity. Some populations form normal bivalents at male meiosis, but 14 populations form chains of chromosomes. Six of these populations form two chains, and so show segregation behaviour which is beyond our current understanding of meiotic processes. Chromosomal variation of this sort is rarely tolerated in other species, because the segregation of long chromosome chains frequently results in gametes with too many or too few chromosomes. The resulting reproductive failure may form the basis for reproductive isolation in many species, and so the mechanisms that allow D. cancerides to segregate long chromosome chains have allowed this species to maintain cohesion despite extensive chromosomal variation over its range. The effect these chromosome chains have on the population genetics of the species is discussed, and a model for the evolution of the system is proposed.     

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.     

Chiasma Repatterning Across a Chromosomal Hybrid Zone Between Chromosomal Races of Mus Musculus Domesticus

Chiasma number and distribution were analysed in male house mice from a karyotypic hybrid zone between the CD race (2n=22) and the standard race (2n=40) located in central Italy. Chiasma repatterning occurs across the transect. The overall trend produces a diminution of chiasmata in the mice with CD chromosomal background. The progressive reduction of chiasmata indicates that genes could pass from one race to another in an asymmetrical way: from metacentric races to the standard population.     

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.     

Chromosomal evidence of incipient speciation in the Afrotropical malaria mosquito Anopheles funestus

The analysis of chromosomal polymorphism of paracentric inversions in anopheline mosquitoes has often been instrumental to the discovery of sibling species complexes and intraspecific genetic heterogeneities associated with incipient speciation processes. To investigate the population structure of Anopheles funestus Giles (Diptera: Culicidae), one of the three most important vectors of human malaria in sub-Saharan Africa, a three-year survey of chromosomal polymorphism was carried out on 4,638 karyotyped females collected indoors and outdoors from two villages of central Burkina Faso. Large and temporally stable departures from Hardy-Weinberg equilibrium due to significant deficits of heterokaryotypes were found irrespective of the place of capture, and of the spatial and temporal units chosen for the analysis. Significant linkage disequilibrium was observed among inversion systems on independently assorting chromosomal arms, indicating the existence of assortative mating phenomena. Results were consistent with the existence of two chromosomal forms characterized by contrasting degrees of inversion polymorphism maintained by limitations to gene flow. This hypothesis was supported by the reestablishment of Hardy-Weinberg and linkage equilibria when individual specimens were assigned to each chromosomal form according to two different algorithms. This pattern of chromosomal variability is suggestive of an incipient speciation process in An. funestus populations from Burkina Faso.     

Studies on the Robertsonian chromosomal variation of Mus musculus domesticus (Rodentia, Muridae) in Greece

The karyotype of the house mouse, Mus musculus domesticus , was examined in 282 specimens from 44 localities, in an effort to gain better understanding of the Robertsonian (Rb) variation known to exist in Greece. We consider that an Rb system exists in Peloponnisos, southern Greece, distributed in an area that is substantially larger than previously known. It consists of at least three Rb races with 2 n  = 30, 2 n  = 24 and 2 n  = 28, respectively, the last being reported for the first time in this paper and carrying Rb(3.6), Rb(8.12), Rb(10.14), Rb(13.15), Rb(9.16) and Rb(11.17) in a homozygous state. Additional instances of variation in this Rb system include individuals with 2 n  = 31 and 32 of variable Rb constitution and hybrids between the Rb races with 2 n  = 30 and 2 n  = 24. In southern Peloponnisos, Rb(10.14) was found in either a homozygous or a heterozygous state (2 n  = 38 or 39). The relationships among the Rb populations of Peloponnisos are discussed and hypotheses for their evolution are proposed. Rb variation was also recorded in two new locations of eastern Sterea Ellas (2 n  = 28 and 29) and one in Ipiros, north-west Greece (2 n  = 38). These findings corroborate the existence of two separate Rb systems in those two areas. Moreover, among a number of islands surveyed, Rb variation was only found in Kythira island, with Rb(10.14) in a heterozygous state (2 n  = 39). Finally, the typical all-acrocentric karyotype (2 n  = 40) was found in 51 of the animals studied from 13 localities. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 503–513.     

REDUCED GENE FLOW AT PERICENTROMERIC LOCI IN A HYBRID ZONE INVOLVING CHROMOSOMAL RACES OF THE HOUSE MOUSE MUS MUSCULUS DOMESTICUS

The West European house mouse, Mus musculus domesticus, is a particularly suitable model to investigate the role of chromosomal rearrangements in reproductive isolation. In fact, it exhibits a broad range of chromosomal polymorphism due to Robertsonian (Rb) fusions leading to various types of contact zones between different chromosomal races. In the present study, we analyzed a parapatric contact in central Italy between the Cittaducale chromosomal race (CD: 2n= 22) and the surrounding populations with standard karyotype (2n= 40) to understand if Rb fusions play a causative role in speciation. One hundred forty‐seven mice from 17 localities were genotyped by means of 12 microsatellite loci. A telomeric and a pericentromeric locus situated on six chromosome arms (four Rbs and one telocentric) were selected to detect differences in the amount of gene flow for each locus in different chromosomal positions. The analyses performed on the two subsets of loci show differences in the level of gene flow, which is more restricted near the centromeres of Rb chromosomes. This effect is less pronounced in the homozygotes populations settled at the border of the hybrid zone. We discuss the possible cause of the differential porosity of gene flow in Rbs considering “hybrid dysfunctions” and “suppressed recombination” models.     

A role for the mismatch repair system during incipient speciation in Saccharomyces

The cause of reproductive isolation between biological species is a major issue in the field of biology. Most explanations of hybrid sterility require either genetic incompatibilities between nascent species or gross physical imbalances between their chromosomes, such as rearrangements or ploidy changes. An alternative possibility is that genomes become incompatible at a molecular level, dependent on interactions between primary DNA sequences. The mismatch repair system has previously been shown to contribute to sterility in a hybrid between established yeast species by preventing successful meiotic crossing-over leading to aneuploidy. This system could also promote or reinforce the formation of new species in a similar manner, by making diverging genomes incompatible in meiosis. To test this possibility we crossed yeast strains of the same species but from diverse historical or geographic sources. We show that these crosses are partially sterile and present evidence that the mismatch repair system is largely responsible for this sterility.     

The genetics and ecology of sympatric speciation: A case study

Mating occurs on the larval host plant in allRhagoletis species (Diptera: Tephritidae). We show how this attribute, when coupled with certain differences in other biological traits, strongly influences the mode of speciation. In species of thesuavis species group, host shifts have never occurred during speciation, and larvae feed in the husks of any walnut species(Juglans spp.), which are highly toxic. Taxa are allopatric or parapatric and exhibit deep phylogenetic nodes suggesting relatively ancient speciation events. Traits responsible for species and mate recognition, particularly in parapatric species, are morphologically distinct and strongly sexually dimorphic. All aspects of their biology, genetics and distribution are consistent with a slow rate of allopatric speciation followed by morphological divergence in secondary contact. In contrast, speciation in thepomonella species group has always involved a shift to a new, usually unrelated, non-toxic host, and all taxa within these groups are sympatric, monophagous and morphologically indistinguishable from one another. Phylogenetic nodes are very shallow, indicating recent sympatric speciation. Sympatric divergence is promoted by genetic variation which allows a portion of the original species to shift to a new habitat or host. Evidence suggests that changes in a few key loci responsible for host selection and fitness on a new host may initiate host shifts. By exploiting different habitats, competition for resources between diverging populations is reduced or avoided. We provide evidence that in phytophagous and parasitic insects sufficient intrinsic barriers to gene flow can evolve between sister populations as they adapt to different habitats or hosts to allow each population to establish independent evolutionary lineages in sympatry.     

The Essential Function of SETDB1 in Homologous Chromosome Pairing and Synapsis during Meiosis

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Variation and Evolution in the Karyotype of Lycoris (Amaryllidaceae) V. Chromosomal Variation in L. sanguinea Maxim.

Abstract In 554 bulbs from 38 populations of Lycoris sanguinea , several chromosomal variations have been discovered. Most of the bulbs have a common karyotype consisting of 22 acrocentric ( A ) chromosomes. Though their frequencies are low, some rearranged chromosomes which are aberrant have been found. The aberrants are as follows: 1. Subtelocentrics ( ST ); 2. Telocentrics ( T' ); 3. Metacentrics ( M' ); 4. Very small acrocentrics (a); 5. Very small metacentrics (m); 6. Acentric fragments ( Ac ); and 7. Dicentrics ( Di ) chromosome. All can be easily suspected to be derived from A s. Some aberrations of the satellite chromosomes have been observed also. In addition, a new karyotype composed of 2n=32=31 A + 1 M' chromosomes has been found.     

Meiosis and the Neo- XY system of Dichroplus vittatus (Melanoplinae, Acrididae): a comparison between sexes

The origin of neo-XY sex systems in Acrididae is usually explained through an X-autosome centric fusion, and the behaviour of the neo-sex chromosomes has been solely studied in males. In this paper we analysed male and female Dichroplus vittatus. The karyotype comprises 2n = 20 chromosomes including 9 pairs of autosomes and a sex chromosome pair that includes a large metacentric neo-X and a small telocentric neo-Y. We compared the meiotic behaviour of the sex bivalent between both sexes. Mean cell autosomal chiasma frequency was low in both sexes and slightly but significantly higher in males than in females. Chiasma frequency of females increased significantly when the sex-bivalent was included. Chiasma distribution was basically distal in both sexes. Behaviour of the neo-XY pair is complex as a priori suggested by its structure, which was analysed in mitosis and meiosis of diploid and polyploid cells. During meiosis, orientation of the neo-XY is highly irregular; only 21% of the metaphase I spermatocytes show standard orientation. In the rest of cells, the alternate or simultaneous activity of an extra kinetochore in the distal end of the short arm (XL) of the neo-X, determined unusual MI orientations and a high frequency of non-disjunction and lagging of the sex-chromosomes. In females, the neo-XX bivalent had a more regular behaviour but showed 17% asynapsis in the XL arm which, in those cases orientated its distal ends towards opposite spindle poles suggesting, again, the activity of a second kinetochore. The dicentric nature and the unstable meiotic behaviour of the sex neo-chromosomes of D. vittatus suggest a recent origin of the sex determination mechanism, with presumable adaptive advantages which could compensate their potential negative heterosis. Our observations suggest that the origin of the neo-sex system was a tandem fusion of two original telocentric X-chromosomes followed by another tandem fusion with the small megameric bivalent and a further pericentric inversion of the neo-X. The remaining autosomal homolog resulted in the neo-Y chromosome. This revised version was published online in July 2006 with corrections to the Cover Date.     

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.     

Along the speciation continuum in sticklebacks

Speciation can be viewed as a continuum, potentially divisible into several states: (1) continuous variation within panmictic populations, (2) partially discontinuous variation with minor reproductive isolation, (3) strongly discontinuous variation with strong but reversible reproductive isolation and (4) complete and irreversible reproductive isolation. Research on sticklebacks (Gasterosteidae) reveals factors that influence progress back and forth along this continuum, as well as transitions between the states. Most populations exist in state 1, even though some of these show evidence of disruptive selection and positive assortative mating. Transitions to state 2 seem to usually involve strong divergent selection coupled with at least a bit of geographic separation, such as parapatry (e.g. lake and stream pairs and mud and lava pairs) or allopatry (e.g. different lakes). Transitions to state 3 can occur when allopatric or parapatric populations that evolved under strong divergent selection come into secondary contact (most obviously the sympatric benthic and limnetic pairs), but might also occur between populations that remained in parapatry or allopatry. Transitions to state 4 might be decoupled from these selective processes, because the known situations of complete, or nearly complete, reproductive isolation (Japan Sea and Pacific Ocean pair and the recognized gasterosteid species) are always associated with chromosomal rearrangements and environment‐independent genetic incompatibilities. Research on sticklebacks has thus revealed complex and shifting interactions between selection, adaptation, mutation and geography during the course of speciation.     

A Transcriptome-based Perspective of Meiosis in Dinoflagellates

There is increasing interest in the possibility of sexual recombination in dinoflagellates, especially those symbiotic with coral, since recombination may be able to augment genetic diversity and reduce levels of coral bleaching. Several previous studies have addressed this in Symbiodinium by querying sequence databanks with a list of 51 genes termed a meiosis detection toolkit. Here, we have constructed an expanded list of 307 genes involved in meiosis in budding yeast. We find the genes involved in the major regulatory steps in yeast meiosis are also found in dinoflagellates, as are many of the genes involved in recombination. In contrast, few genes involved in forming the synaptonemal complex or forming spores are conserved. We further note that the meiosis-related genes absent in dinoflagellates are also as a general rule absent from other protists in the closely related apicomplexa and the ciliates. We conclude the symbiotic dinoflagellates are as able to undergo meiosis as are other protists.     

Continuing studies on chromosomal polymorphism in a Korean natural population of Drosophila melanogaster

Investigations on the chromosomal inversion polymorphism were conducted on a Korean (Taenung) natural population of D. melanogaster during the period 1978 to 1992. A total of 66 different endemic and cosmopolitan inversions were found on both major chromosome pairs II and III. Some of them proved to be rare cosmopolitan types (2LKA, 2LNS, 2LF, 2RCy, 3LM, 3RKI, and 3RK), while others were endemics. The distribution of breakpoints for endemic and rare cosmopolitan inversions are not random along the two autosome arms.With respect to frequency changes, the 15-year survey revealed that five of the cosmopolitan types (2Lt, 2RNS, 3LP, 3RC, and 3RMo) exhibit cyclical frequency changes, whereas gene arrangement 3RP shows relatively stable frequencies. Tests for correlations between gene arrangement frequencies and several climatic variables gave no clear evidence for such relationships. Only one correlation coefficient out of 64 was statistically significant. This revised version was published online in July 2006 with corrections to the Cover Date.     

Homoploid hybrid speciation and genome evolution via chromosome sorting

Genomes of numerous diploid plant and animal species possess traces of interspecific crosses, and many researches consider them as support for homoploid hybrid speciation (HHS), a process by which a new reproductively isolated species arises through hybridization and combination of parts of the parental genomes, but without an increase in ploidy. However, convincing evidence for a creative role of hybridization in the origin of reproductive isolation between hybrid and parental forms is extremely limited. Here, through studying Agrodiaetus butterflies, we provide proof of a previously unknown mode of HHS based on the formation of post-zygotic reproductive isolation via hybridization of chromosomally divergent parental species and subsequent fixation of a novel combination of chromosome fusions/fissions in hybrid descendants. We show that meiotic segregation, operating in the hybrid lineage, resulted in the formation of a new diploid genome, drastically rearranged in terms of chromosome number. We also demonstrate that during the heterozygous stage of the hybrid species formation, recombination was limited between rearranged chromosomes of different parental origin, representing evidence that the reproductive isolation was a direct consequence of hybridization.     

Population genetics of speciation in nonmodel organisms: I. Ancestral polymorphism in mangroves

The level of DNA polymorphism in the ancestral species at the time of speciation can be estimated using DNA sequences from many loci sampled from 2 or more extant species. The comparison between ancestral and extant polymorphism can be informative about the population genetics of speciation. In this study, we collected and analyzed DNA sequences of approximately 60 genes from 4 species of Sonneratia, a common genus of mangroves on the Indo-Pacific coasts. We found that the 3 ancestral species were comparable to each other in terms of level of polymorphism. However, the ancestral species at the time of speciation were substantially more polymorphic than the extant geographical populations. This ancestral polymorphism is in fact larger than, or at least equal to, the level of polymorphism of the entire species across extant geographical populations. The observations are not fully compatible with speciation by strict allopatry. We suggest that, at the time of speciation, the ancestral species consisted of interconnected but strongly divided geographical populations. This population structure would give rise to high level of polymorphism across species range. This approach of studying the speciation history by genomic means should be applicable to nonmodel organisms.