Maintaining genetic integrity with high promiscuity: Frequent hybridization with low introgression in multiple hybrid zones of Melocactus (Cactaceae)

Khan, Gulzar; Franco, Fernando Faria; Silva, Gislaine A. R.; Bombonato, Juliana Rodrigues; Machado, Marlon C.; Alonso, Diego Peres; Ribolla, Paulo Eduardo Martins; Albach, Dirk C.; Moraes, Evandro M.

doi:10.1016/j.ympev.2019.106642

Cited by 20 publications

(18 citation statements)

References 57 publications

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“…However, a directly contrasting outcome of hybridization is evident in another cactus genus found in the rocky outcrops of the Morro do Chapéu in the Brazilian caatinga. Khan et al (2020) used RADseq data to show that, despite extensive hybridization between five species of Melocactus Link & Otto in a hybrid zone, there were extremely low levels of introgression coupled with strong selection against hybrids, building on previous morphological and allozyme evidence of hybridization in other Melocactus spp. (Lambert et al, 2006).…”

Section: Deserts and Tropical Dry Forestsmentioning

confidence: 99%

“…For example, in C 4 and non-C 4 forms of the grass Alloteropsis semialata (R.Br.) Hitchc., hybridization has been shown to occur, but hybrids are usually selected against (as in Melocactus; Khan et al, 2020). It is likely that this barrier, coupled with different ploidies among forms, has allowed co-existence and maintained reproductive boundaries after the forms came into secondary contact following re-expansion of Miombo woodlands (Olofsson et al, 2021).…”

Section: Hybridization In the Neotropics Vs Other Tropical Regionsmentioning

confidence: 99%

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Hybridization: a ‘double-edged sword’ for Neotropical plant diversity

Schley

Twyford

Pennington

2021

Botanical Journal of the Linnean Society

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Hybridization can facilitate both evolutionary diversification and extinction and has had a critical role in plant evolution, with c. 25% of species known to hybridize in some temperate floras. However, in the species-rich Neotropical flora, the role of hybridization in the evolution of diversity remains unclear. Our review examines studies of hybridization in seed plants from across the Neotropics and explores its outcomes on Neotropical plant evolution. We review studies on a per-biome basis and a spectrum of evolutionary outcomes from hybridization are evident across Neotropical biomes and taxa. These range from short-term impacts, such as the broadening of ecological amplitude in hybrid progeny with transgressive phenotypes and genetic swamping, through to long term impacts, such as the generation of new lineages. Among these studies certain themes emerge, such as the pervasive hybridization among species-rich plant radiations from the Andean páramos, suggesting a role for hybridization in rapid diversification events. Finally, we highlight that hybridization is relatively understudied in the Neotropical flora, despite its remarkable species richness. The advent of genomic techniques can facilitate the study of hybridization and its effects in understudied biomes and plant groups. The increasing availability of genomic resources will eventually allow comparisons between tropical and temperate floras and therefore shed light on the evolutionary impacts of hybridization across the latitudinal biodiversity gradient.

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Section: Deserts and Tropical Dry Forestsmentioning

confidence: 99%

Section: Hybridization In the Neotropics Vs Other Tropical Regionsmentioning

confidence: 99%

Hybridization: a ‘double-edged sword’ for Neotropical plant diversity

Schley

Twyford

Pennington

2021

Botanical Journal of the Linnean Society

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“…Lastly, we counted the introgressed loci from the observed hybrid genotypes by comparing with the probability densities of homozygotes and heterozygotes genotypes as suggested (Nolte et al, 2009). We adjusted the neutral expectation of genomic clines through multiple comparisons using the false discovery rate (FDR) as suggested (Benjamin and Hochberg, 1995;examples in Harrison et al, 2017;Khan et al, 2020).…”

Section: Characterization Of Hybrids Classes and Introgressionmentioning

confidence: 99%

Comparative Phylogeography of Veronica spicata and V. longifolia (Plantaginaceae) Across Europe: Integrating Hybridization and Polyploidy in Phylogeography

et al. 2021

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Climatic fluctuations in the Pleistocene caused glacial expansion-contraction cycles in Eurasia and other parts of the world. Consequences of these cycles, such as population expansion and subsequent subdivision, have been studied in many taxa at intraspecific population level across much of the Northern Hemisphere. However, the consequences for the potential of hybridization and polyploidization are poorly understood. Here, we investigated the phylogeographic structure of two widespread, closely related species, Veronica spicata and Veronica longifolia, across their European distribution ranges. We assessed the extent and the geographic pattern of polyploidization in both species and hybridization between them. We used genome-scale SNP data to clarify phylogenetic relationships and detect possible hybridization/introgression events. In addition, crossing experiments were performed in different combination between V. spicata and V. longifolia individuals of two ploidy levels and of different geographic origins. Finally, we employed ecological niche modeling to infer macroclimatic differences between both species and both ploidy levels. We found a clear genetic structure reflecting the geographical distribution patterns in both species, with V. spicata showing higher genetic differentiation than V. longifolia. We retrieved significant signals of hybridization and introgression in natural populations from the genetic data and corroborated this with crossing experiments. However, there were no clear phylogeographic patterns and unequivocal macroclimatic niche differences between diploid and tetraploid lineages. This favors the hypothesis, that autopolyploidization has happened frequently and in different regions. The crossing experiments produced viable hybrids when the crosses were made between plants of the same ploidy levels but not in the interploidy crosses. The results suggest that hybridization occurs across the overlapping areas of natural distribution ranges of both species, with apparently directional introgression from V. spicata to V. longifolia. Nevertheless, the two species maintain their species-level separation due to their adaptation to different habitats and spatial isolation rather than reproductive isolation.

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“…Here we extended the previous study by using double-digest restriction site-associated DNA (ddRAD) sequencing to quantify the extent of hybridization in this hybrid zone. Double-digest restriction site-associated DNA can generate massive genome-wide single-nucleotide polymorphism (SNP) data sets, without any prior genomic information, thus making it widely applied to evolutionary studies involving resolving long-standing taxonomic problems, species boundaries in taxonomically complex groups, population genetics and phylogenetic research ( Wagner et al 2017 , 2020 ; Spriggs et al 2019 ; Khan et al 2020 ). Two taxa were included in this study: Cremanthodium stenoglossum grows mainly at an altitude of 3700–5000 m in the southern part of Qinghai province and northwest Sichuan province, while Ligularia nelumbifolia mainly occurs at an altitude of 2400–3900 m in Northwest to Northeast Yunnan, Southwest to Northwest Sichuan, West Hubei and Southwest Gansu ( Chen et al 2011 ).…”

Section: Introductionmentioning

confidence: 99%

The natural hybridization between speciesLigularia nelumbifoliaandCremanthodium stenoglossum(Senecioneae, Asteraceae) suggests underdeveloped reproductive isolation and ambiguous intergeneric boundary

Yang

Wang

et al. 2021

AoB PLANTS

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Natural hybridization is frequent in plants and is considered an important factor facilitating speciation. The natural intergeneric hybridization between Ligularia and Cremanthodium was previously confirmed using a couple of DNA markers. However, the mechanism of this intergeneric hybridization and the role of reproductive isolation in the process of hybridization remain unclear. Here we used double digest restriction-site associated DNA sequencing (ddRAD-Seq) to further quantify the occurrence of hybridization, the genetic structure of the hybrid population and the role of reproductive isolation between Ligularia nelumbifolia and Cremanthodium stenoglossum. The results based on the ddRAD-seq SNP datasets indicated that hybridization between L. nelumbifolia and C. stenoglossum was restricted to F1s, and no gene introgression was identified between these two species. STRUCTURE analysis and ML tree results showed a slightly larger genetic contribution of L. nelumbifolia to putative hybrid F1s. We deduced that the reproductive isolation between these two parent species is not well developed but still strong enough to maintain the genetic integrity of the species, and that their F1s are sterile or with low fertility. Given the poorly resolved phylogenetic relationship between Ligularia and Cremanthodium, the occurrence of natural hybridization between L. nelumbifolia and C. stenoglossum may provide new insights into the re-circumscription and re-delimitation of these two genera.

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Maintaining genetic integrity with high promiscuity: Frequent hybridization with low introgression in multiple hybrid zones of Melocactus (Cactaceae)

Cited by 20 publications

References 57 publications

Hybridization: a ‘double-edged sword’ for Neotropical plant diversity

Hybridization: a ‘double-edged sword’ for Neotropical plant diversity

Comparative Phylogeography of Veronica spicata and V. longifolia (Plantaginaceae) Across Europe: Integrating Hybridization and Polyploidy in Phylogeography

The natural hybridization between speciesLigularia nelumbifoliaandCremanthodium stenoglossum(Senecioneae, Asteraceae) suggests underdeveloped reproductive isolation and ambiguous intergeneric boundary

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