The role of chromosome rearrangements in reproductive isolation and speciation: PLANTS Coghlan et al. (2005) Are chromosomal rearrangements merely a problem for the genome, or do they have functional significance in the short term (e.g. by enabling a species to adapt to changing environmental conditions) or in the long term (e.g. by facilitating speciation)? Chromosome mutations are variations in: 1. Chromosome structure (chromosomal rearrangements) deletions duplications • translocations • inversions .__________________________________________________________________«< • transpositions mostly due to errors or mispairings in crossing over 2. Chromosome number • aneuploidy • abnormal euploidy When chromosome rearrangements occur they are rare in a population: How do they spread? Problems Both morphologically distinct species that lack chromosomal differences (e.g. translocations and inversions) and morphologically cryptic species with chromosomal differences can be found 0- The amount of phenotypic evolution is not a good predictor of the amount of karyotypic evolution Are chromosome rearrangements important for creating reproductive isolation barriers and speciation? Is the accumulation of chromosomal differences between populations largely incidental to speciation? More problems... • newly arisen chromosomal rearrangements will exist in the population almost exclusively as heterozygotes (inversion or translocation heterozygotes) • many chromosomal rearrangements have little effect on fertility (ineffectiveness of chromosomal differences as barriers to gene flow) • novel chromosomal arrangements have a selective disadvantage when they first appear in a population: the problem of underdominance: difficulties associated with fixing chromosomal rearrangements that are strongly underdominant (i.e. reduce the fitness of heterozygotes) Models of chromosomal speciation (Rieseberg 2001) » Chain or Cascade modeis Chromosomal transilience model Monobrachial fusion model Recombinational model Quantum speciation model Stasipatric model V • Saltational model References White, M.J.D. (1978) Modes of Speciation. Templeton, A.R. (1981) Mechanisms of speciation - a population genetic approach. Annu. Rev. Ecol. Syst. 12, 23-48. Baker, R.J. and Bickham J.W. (1986) Speciation by monobrachial centric fusions. Proc. Natl. Acad. Sei. U. S. A. 83, 8245-8248. Grant, V. (1981) Plant Speciation. Lewis, H. (1966) Speciation in flowering plants. Science 152,167-172. Fundamental feature of the models: chromosomal differences that have accumulated between the neospecies and its progenitor(s) are assumed to impair the fertility or viability of interspecific hybrids, thereby reducing gene flow Deviating features of the models: • geographical isolation is (not) required for speciation • the means by which chromosomal rearrangements arise and become fixed • effects of rearrangements on the fitness of chromosomally heterozygous individuals Suppressed-recombination model (Rieseberg 2001, Noor et al. 2001) Drosophila • inversions have contributed to speciation between the close relatives D. pseudoobscura and D. persimilis. inversions are found within the genomic regions associated with hybrid sterility • chromosomal rearrangements reduce recombination between the genomes of the species, thereby enabling genetic differences to accumulate within the rearranged regions • inversions are more common between Drosophila species that are sympatric compared to allopatric pairs Chromosome spec ration in brosophila • gross chromosomal rearrangement in Drosophila are well characterized as they are easily detected in the chromosomes of their giant salivary glands • the most common type of gross chromosomal rearrangement are paracentric inversions (do not span the centromere) • paracentric inversions are common polymorphisms in drosophilas and other fly species (different populations of D. me/anogasterharbor more than 500 inversion polymorphisms) HGFFDC B A Do chromosomal rearrangements contribute to speciation in Anopheles gambiae? (a) Polymorphic inversions in A. gambiae 2R 2RI -tf 2Rj 2Rb 2Rbk 2^d 2 Re 2Ru (b) Inversion genotypes of n on-interbreeding populations in Mali -/V Bamako; 2R jou or 2R jbcu -^V MoPti■ 2F icor2l uor2l (standard) -^ŕ Savanna :2R b or 2R cu or 2R bcu or 2R + TRENDS m Genetics (a) The main polymorphic paracentric inversions in A. gambiae chromosome arm 2R. (b) Three non-interbreeding populations of A. gambiae (named Bamako, Savanna and Mopti) that live in the same region of Mali. The three populations differ by chromosomal inversions that might be contributing to speciation in A. gambiae. For example, a chromosome with arrangement 2Rjcu has inversions], c and u. The role of chromosomal rearrangements in speciation in the A. gambiae species complex is difficult to prove: even a highly significant coincidence in time between chromosomal rearrangements and speciation does not prove a causal relationship. Suppressed-recombination model (Rieseberg 2001, Noorer 0/2001) PLANTS • the exact relationship between chromosomal rearrangement and speciation remains unclear in plants! • seems that sunflowers {Helianthuš) are only example: recombination between two divergent diploid species appears to have provoked speciation events in sunflowers (Loren Rieseberg's lab) Suppressed-recombination model (Rieseberg 2001, Noor eta/. 2001) Chromosome rearrangements provide large regions of the genome protected from gene flow where isolating genes may accumulate until complete reproductive barriers exist. The model suggests that rearrangements may reduce gene flow more by suppressing recombination than by directly reducing fitness. Unlike other models of chromosomal speciation, the suppressed-recombination model does not suffer from the problem of underdominance. A secondary contact scenario: chromosomal rearrangements favor speciation because they impede introgression across a large block of the genome, thus allowing certain chromosomal regions of two hybridizing populations to persist without fusing longer than regions where no chromosomal changes were present. ^ Hybrid Homoploid y speciation in sunflowers (Helianthus) Chromosomal Recombinational j > hybrid or recombinational speciation refers to the origin of a new homoploid species wä hybridization between chromosomally or genetically divergent parental species > homoploid hybrid speciation is theoretically difficult because it requires the development of reproductive barriers in sympatry or parapatry (the possibility of backcrossing with their parental species) > theory suggests that isolation may arise through rapid karyotypic evolution and/or ecological and spatial divergence of hybrid neospecies > it is assumed that new hybrid lineage diverge karyotypically from its parental species through the chromosomal rearrangements that differentiate the parental species and/or by new chromosomal rearrangements induced by recombination > three Helianthusspecies are probably the best documented examples of homoploid hybrid speciation in either animals or plants Homoploid hybrid speciation in sunflowers (Helianthus) all diploid (n=17), annual and self-incompatible H. annuus x H. petiolans V H. anomalus H. deserticola H. paradoxus W. * j JW** |*l*; : annuus( 'jj^i^iliH By j| # three different hybrid species occupying different habitats *,. u paraaoxus- anomalus (hybrid) geserticola (h^rjfl) (hybrid) f Helianthus annuus ■2.1* * \ Bfi PO r--**/ Helianthus petiolaris Helianthus anomalus Homoploid hybrid speciation: H. anomalus • a sand dune endemic, central Utah and northern Arizona • both parental species are widespread; hybridize but retain their genetic integrity because of the synergistic action of several reproductive barriers • three experimentally generated hybrid lineages (//. annuusx H. petiolariš) showed a combination of chromosomal blocks similar to that found in H. anomalus (Rieseberg et al. 1996) • the three synthetic lineages were cross-compatible with each other and with H. anomalus (Rieseberg 2000) • H. anomalus has diverged considerably from its parents in both karyotype and ecological preference due to the sorting of chromosomal rearrangements that differentiate the parental species. H. anomalus also possesses several unique arrangements, possibly induced by recombination. As a result, H. anomalus is almost completely intersterile with its parental species H. crnnuus x H. petiolariš v H. anomalus Reccurent origin of H. anomalus ? • documentation of the multiple origins of diploid hybrid species is difficult • introgression following a hybrid origin may produce patterns that are almost indistinguishable from those produced by recurrent hybrid speciation S greenhouse experiments showed that the genomic composition of hybrid lineages is shaped in part by deterministic forces S recurrent diploid hybrid speciation may be more feasible than previously believed S chloroplast DNA (cpDNA) and crossability data were most consistent with a scenario in which H. anomalus arose three times: three different H. anomalus fertility groups were discovered, each with a unique cpDNA haplotype Comparative genetics in five Helianthus species Comparative genetic mapping in plants Analyzing karyotypic changes Cytology - chromosome structure/morphology and chromosome pairing in meiosis I Limitations • indistinguishable chromosomes • disruption of meiotic pairing; ambigious interpretations of meiotic configurations Comparative genetic (linkage) mapping (1988: first comparative studies published) s based on inter-species mapping of known orthologous sequences s allows comparisons to be made between species, genera, and even families (difficult by cytological analysis) Limitations • the quality of a genetic map depends on marker density • large-scale rearrangements are readily detected, whereas those involving small chromosomal segments are likely to go undetected Inferred chromosomal structural relationships between the parental species, H. annuus and H. petiolaris, and their three diploid hybrid derivatives, H. anomalus, H. deserticola, and H. paradoxus ANN ANO DES PAR PET š 3 3 o 3 ANN AND DES PAR PET 1 1 < Ti 1 1 PA^ ANN ANO DES PAR PET ANN ANO DES PAR PET DES PAR PET 1 ■■2 < O 'J § s O -; -; s It Li ■=: '.JJ ■í ■D '3 AMN ANO DES PAR PET ANN ANO DES PAR PET -J ANN ANO DES PET ANN ANO DES PAR PET U u ANN ANO DES PAR PET 1 1 •■D 2 ■C -■"i i] ■.r ú 3 * 1 o o o £■ u? o Ľ ANN ANO DES PAR PET ANN ANO DES PAR PET ANNJ ANO DES PAR PET ANN AHO DES PAR PET ANN ANO DES PAP PET ANN ANO DES PAR PET ANN ANO DES PAR PET ANN ANQ DES PAF| PET 1 ■i J -3 * -n 3 u -o 5 AHN ANO DES PAR PET Segments containing inversions are indicated by hatched lines ANN ANO DCS PAR PET ANN ANO DES PAR FET C/) O a> (D O lO o o CM "ČO (D (Č Inferred chromosomal structural relationships between the parental species, H. annuus and H. petiolaris, and their three diploid hybrid derivatives, H. anomalus, H. deserticola, and H. paradoxus ANN ANO DES PAR PET ANN ANO DES PAR PET ANN DES PAR PET o 3 1 o 3 T" *: ■ŕ-__i -i ■■; 'J ____i v: 'í C- 'ľ C- c -; t: í." — ■c Ü0 ■D O U ____i -I ____i ANN ANO DES PAR PET U u ANN ANO DES PAR PET ANN ANO DES PAR PET u-o _ 2i ■... o--o O __i o __i Lai etal. 2005, Genetics 171 Homoploid hybrid speciation in sunflowers (Helianfhus) > it is assumed that new hybrid lineage diverge karyotypically from its parental species through the chromosomal rearrangements that differentiate the parental species and/or by new chromosomal rearrangements induced by recombination • karyotypes of the three hybrid species are massively divergent from their parental species • about one-third of the karyoypic differences arose through the sorting of parental chromosomal rearrangements • the remainder of karyotypic differences appear to have arisen de novo (6 breakages/6 fusions in H. anomalus, 4 breakages/3 fusions in H. deserticola, and 5 breakages/5 fusions in H. paradoxus) • karyotypic differences contribute to reproductive isolation: 9 of 11 pollen viability QTLs occur on rearranged chromosomes and all but one map close to a rearrangement breakpoint H. annuus x H. petiolans v H. anomalus H. deserticola H. paradoxus ANN ANO DES PAR PET — " 'N O f» r* < - is ■D 2 0Ü ■x ■Z; •2 Homoploid hybrid speciation in sunflowers (Helianfhus) • approx. 50% of the reproductive barrier between Helianthus species is caused by chromosomal rearrangements __________________________ f \ H. annuus x H. petiolaris • the data in line with the theory (rapid karyotypic evolution in the hybrid sunflowers have facilitated the development of reproductive isolation with their parental species) • the lengths of chromosomal segments around isolating genes that are prevented from introgressing across hybrid zones are longer in rearranged vs. collinear chromosomes In Drosophila, genes causing hybrid sterility and conditioning female species preferences between D. pseudoobscura and D. persimilis map predominantly to inversions that differentiate the species (Noor et al. 2001) V H. anomalus H. deserticola H. paradoxus Genome size increase in hybrid Helianthus species • hybrid-derived species have 50% more nuclear DNA than the parental species (//. annuus andH. petiolariš) • first- and sixth-generation synthetic hybrids and hybrid-zone plants did not show an increase from parental DNA content xz • hybridization by itself does not lead to increased nuclear DNA content in Helianthus • is amplification of repetitive sequences responsible for the increases in DNA content in the hybrid-derived species? Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation Mark C. Ungerer, Suzanne C. Strakosh and Ying Zhen Current Biol 16 (2006' • 3 hybrid species exhibit species-specific karyotypic alterations • all 3 species have at least 50% larger genomes than the parental species • 5.6 to 23.6-fold increases in copy number of the Ty3/gypsy retrotransposon in all hybrid taxa Southern blots probed with an 887 base pair region of the Ty3/§ypsy integrase domain Copy number estimates (per genome) of the Ty3/§ypsy integrase domain based on quantitative PCR V \ ^ \ \ \ ^12 3 4 5 12345 •Mf- 12 3 4 5 2.0kb -£.0kb ■0.6kb '- 23.0kb - 4.4kb - 2.0kb - 0.6kb 360000 E 300000 g 250000 8 I 200000 4. % 150000 & 100000 I § 50000 i-t1 0 m n M O A ab b .n.m, -O.ekb J> J* & jjP jF J> J>