The role of chromosome rearrangements in reproductive isolation and speciation (chromosomal speciation, particularly in 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)? Problems Both morphologically distinct species that lack chromosomal differences (e.g. translocations and inversions) and morphologically cryptic species with chromosomal differences can be found 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? Or is the accumulation of chromosomal differences between populations largely incidental to speciation? (e.g., = speciation → chromosome rearrangements) M.J.D. White YES! Cryptic species with population-specific chromosome rearrangements? Grund et al. 2006, PNAS 103 Draba nivalis See also: Gustafsson ALS, Skrede I, Rowe HC, Gussarova G, Borgen L, et al. (2014) Genetics of Cryptic Speciation within an Arctic Mustard, Draba nivalis. PLoS ONE 9(4): e93834. doi:10.1371/journal.pone.0093834 Grund et al. 2006, PNAS 103: Although 99% of parental individuals were fully fertile, the fertility of intraspecific crosses was surprisingly low. Hybrids from crosses within populations were mostly fertile (63%), but only 8% of the hybrids from crosses within and among geographic regions (Alaska, Greenland, Svalbard, and Norway) were fertile. The frequent occurrence of intraspecific crossing barriers is not accompanied by significant morphological or ecological differentiation, indicating that numerous cryptic biological species have arisen within each taxonomic species despite their recent (Pleistocene) origin. Draba nivalis Cryptic species with population-specific chromosome rearrangements? Models of chromosomal speciation (Rieseberg 2001) • Chain or Cascade models • Chromosomal transilience model • Monobrachial fusion model • Recombinational model • Quantum speciation model • Stasipatric model • 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. Sci. 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 Chromosomal speciation: 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) Two models: o the hybrid-sterility model o recombination-suppression model Chromosomal speciation Suppressed-recombination model (Rieseberg 2001, Noor et al. 2001) Experimental data 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 (also true for butterflies) Plants - the exact relationship between chromosomal rearrangement and speciation remains unclear in plants! ....but it is expected and probable - sunflowers (Helianthus), Mimulus Chromosome rearrangements provide large regions of the genome protected from gene flow where isolating genes may accumulate until complete reproductive barriers exist. Suppressed-recombination model (Rieseberg 2001, Noor et al. 2001, Faria and Navarro 2010) The model suggests that rearrangements may reduce gene flow by suppressing recombination. CRs allow genes located in these regions to differentiate, in contrast to genes in freely recombining collinear regions. A paracentric inversion in D. pseudoobscura • gross chromosomal rearrangements in Drosophila are well characterized as rearrangements 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. melanogaster harbor more than 500 inversion polymorphisms) Chromosome speciation in Drosophila Inversions are crossover suppresors – evolutionary consequences (speciation) Anopheles gambiae (a) 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 3 populations differ by chromosomal inversions that might be contributing to speciation in A. gambiae. (For example, a chromosome with arrangement 2R jcu has inversions j, c and u on chrosmosome arm 2R.) Do chromosomal rearrangements contribute to speciation in Anopheles gambiae? 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. Love et al. (2016), Mol Ecol • initial genomic and ecological differentiation – sympatric speciation • the majority of differentiated regions between Bamako and typical An. gambiae are located inside inversions • differentiated genomic regions were enriched for genes implicated in nervous system development and signalling Bamako Suppressed-recombination model PLANTS • the exact relationship between chromosomal rearrangement and speciation remains unclear in plants! ...but more evidence is emerging (new methods available) • seems that sunflowers (Helianthus) are only example: hybridization between two divergent diploid species appears to have provoked speciation events in sunflowers (Loren Rieseberg’s lab) ....and recently Mimulus guttatus (Lowry and Willis 2010) Hybrid Homoploid Chromosomal Recombinational speciation in sunflowers (Helianthus) The rate of introgression is lower within rearranged chromosomes /chromosome regions (vs. collinear regions). The strongest difference close to the breakpoints - consistent with suppressed-recombination models (the strongest reduction in recombination). Hybrid Homoploid Chromosomal Recombinational ➢ three Helianthus species are probably the best documented examples of homoploid hybrid speciation in either animals or plants ➢ hybrid or recombinational speciation refers to the origin of a new homoploid species via 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 speciation in sunflowers (Helianthus) ➢ 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 Helianthus annuus Helianthus petiolaris Helianthus 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 (H. annuus x H. petiolaris) 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 Homoploid hybrid speciation: H. anomalus H. annuus x H. petiolaris H. anomalus Homoploid hybrid speciation in sunflowers (Helianthus) • 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) ➢ 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 H. annuus x H. petiolaris H. anomalus H. deserticola H. paradoxus • 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 • 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 perennial and annual plant yellow monkeyflower (Mimulus guttatus) M. guttatus: geographic distribution of the chromosomal inversion (A) Map of western North America with the locations of populations of coastal perennials (blue), inland annuals (orange), and inland perennials (purple), as well as obligate self-fertilizing species M. nasutus (yellow). (B) Marker order of the AN and PE inversion arrangements along linkage group eight. Inland annuals and M. nasutus had the AN arrangement while coastal and inland perennials all had the PE arrangement. o a geographically widespread adaptive inversion polymorphism in the yellow monkeyflower (Mimulus guttatus) o the inversion is involved in a classic life-history shift in plants - an adaptive response to differences in the seasonal availability of water resources: - one arrangement of the inverted region is found in an annual ecotype that lives in Mediterranean habitats characterized by reduced soil water availability in the summer; - the other arrangement appears in a perennial ecotype that lives in habitats with high yearround soil moisture. o inversion polymorphism influences morphological and flowering time differences between the two ecotypes = reproductive isolating barriers o observation is consistent with the theory that adaptation to local environments can drive the spread of chromosomal inversions and promote speciation. o for the first time in nature was shown the contribution of an inversion to adaptation, an annual/perennial life-history shift, and multiple reproductive isolating barriers Inversion polymorphism and adaptation in Mimulus Chromosome „fusions“ (CF) as a speciation agent ? Loci A and B segregate independently in unfused homozygotes, recombination has different rates and segregation is different in heterozygotes and fused homozygotes o CF can lead to tight linkage of genes („super-gene“) o ... can avoid recombination between locally adapted alleles – adaptation / divergence / speciation o ... can alter gene expression (silencing or higher expression) o ...can confer mechanistic advantage (decreased no. of chromosomes = faster processes = possible adaptive advantage) Chromosome „fusion“ – the origin of the human (dicentric) chromosome 2 2n = 48 2n = 46 Chromosome „fusion“ – the origin of the human (dicentric) chromosome 2 inactive centromere active centromere Chiatante et al. (2017), MBE Chromosome „fusion“ – the origin of the human (dicentric) chromosome 2 Chiatante et al. (2017), MBE Two options how the „fusion“ chromosome 2 was stabilized • the ancestral centromere (AC) was either epigenetically inactivated or centromeredetermining sequences were excised • the excision is more probable – what mechanism? • recombination-based excision, most likely in one step (similar human clinical cases...) Did the origin of „fusion“ chromosome 2 contributed to reproductive isolation of hominid species from great apes? 2n = 48 2n = 46 • different no. of chromosomes → reproductive isolation • loss of gene(s) → adaptive advantage • gene linkage? changed regulation of gene expression? Potter et al. (2017), Front Genet Chromosomal speciation – example of rock-wallabies Potter et al. (2017), Front Genet Chromosomal speciation – example of rock-wallabies • chromosome „fusions“ via reciprocal translocations • inversions • centromere shifts Speciation by Robertsonia translocations („centric fusions“) Ahola et al., Nat Comm (2014) The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal „fusions“ in Lepidoptera • Lepidoptera: n = 5 to 223 • the ancestral lepidopteran karyotype has been n = 31 for at least 140 million years • karyotype evolution through chromosome „fusions“ When considering all the data, the emerging picture is that evidence for chromosomal speciation varies between lineages. For example, it is strong for Drosophila, but much weaker or absent in primates. The observation that appears most consistently in many species is an increased level of divergence near rearrangement breakpoints. According to suppressed-recombination models, these regions constitute strong candidate regions to accumulate alleles involved in reproductive isolation. Faria and Navarro (2010) The question is, are CRs an important component of speciation?