Hybrid speciation via inheritance of alternate alleles of parental isolating genes

The importance of hybridization in generating biological diversity has been historically controversial. Previously, inference about hybridization was limited by dependence on morphological data; with the advent of the next-generation sequencing tools for nonmodel organisms, the evolutionary significance of hybridization is more evident. Here, we test classic hypotheses of hybrid origins of two species in the Phlox pilosa complex. Morphological intermediacy motivated the hypotheses that Phlox amoena lighthipei and Phlox pilosa deamii were independent homoploid hybrid lineages derived from P. amoena amoena and P. pilosa pilosa. We use double-digest restriction site-associated DNA sequencing of individuals from throughout the range of these taxa to conduct the most thorough analysis of evolutionary history in this system to date. Surprisingly, we find no support for the hybrid origin of P. pilosa deamii or P. amoena lighthipei. Our data do identify a history of admixture in individuals collected at a contemporary hybrid zone between the putative parent lineages. We show that three very different evolutionary histories, only one of which involves hybrid origin, have produced intermediate or recombinant morphological traits between P. amoena amoena and P. pilosa pilosa. Although morphological data are still an efficient means of generating hypotheses about past gene flow, genomic data are now the standard of evidence for elucidating evolutionary history.

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“…2016; Wang et al. 2021). However, in many cases where natural hybridization has been identified, its consequences remain unknown.…”

Section: Figurementioning

confidence: 99%

Genomic analyses overturn two long‐standing homoploid hybrid speciation hypotheses

2021

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“…However, occasional interspecific gene flow through long‐distance dispersal and range shift by climate oscillation might have led to the origin of hybrid species through polyploidization (allopolyploidization) or hybridization at the same ploidy level (Homoploid hybrid speciation, HHS). One HHS species may inherit alternative alleles of two parents at reproductive isolation (RI) and phenotype loci, to produce an initial RI and an intermediate phenotype (Wang et al, 2021). In addition, interspecific hybrids and/or introgressed populations commonly exist in the field for numerous groups (Wang et al, 2019, 2021; Ma et al, 2019; Feng et al, 2019; Li et al, 2020, 2021a; Mao et al, 2021) because most of these species are still on the speciation track without full RI (Liu, 2016).…”

Section: Species Diversification In the Qtpslmentioning

confidence: 99%

“…One HHS species may inherit alternative alleles of two parents at reproductive isolation (RI) and phenotype loci, to produce an initial RI and an intermediate phenotype (Wang et al, 2021). In addition, interspecific hybrids and/or introgressed populations commonly exist in the field for numerous groups (Wang et al, 2019, 2021; Ma et al, 2019; Feng et al, 2019; Li et al, 2020, 2021a; Mao et al, 2021) because most of these species are still on the speciation track without full RI (Liu, 2016). Similar to the other mountainous biodiversity hotspots (Flantua et al, 2019; Rahbek et al, 2019a), strong geographic isolation and hybridization may have together played an important role in creating the high species diversity in the QTP sl .…”

Section: Species Diversification In the Qtpslmentioning

confidence: 99%

“…For such research, causal correlations between genetic variation and phenotype could be tested by population genomic data and biochemical and molecular experiments. These genetic mechanisms and key genes underlying environmental adaptation and speciation will undoubtedly deepen our understanding of biodiversity evolution in this region (Wang et al, 2021).…”

Section: Recommendations For Future Researchmentioning

confidence: 99%

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Evolutionary origin of species diversity on the Qinghai–Tibet Plateau

Mao

Wang

Liu

2021

J of Sytematics Evolution

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The Qinghai–Tibet Plateau (QTP) sensu lato (sl) houses an exceptional species diversity in Asia. To develop a comprehensive understanding of species diversity in this fascinating region, we reviewed recent progress from biogeographic, paleogeographic, paleontological and genomic research of both plants and animals in the QTPsl. Numerous studies have been conducted to examine whether the QTPsl uplift triggered the production of rich species diversity there, whether a Quaternary “unified ice sheet” eliminated plants and animals on the central plateau and how high‐altitude species developed the extreme environment adaptations. Major disputes arose about the first issue, mainly from different understanding of the QTP circumscriptions and related uplift, inaccurate dating of molecular phylogenetic trees, and non‐causal correlations between uplift and species diversification. The QTPsl uplift is spatially and temporally heterogeneous, and abundant fossils reported recently similarly support such an asynchronous upheaval model across the entire region. Available phylogeographic studies of alpine plants and animals suggested their glacial refugia in the central QTPsl, rejecting a unified ice sheet during the Last Glacial Maximum. Genomic evidence from a limited number of alpine species has identified numerous candidate genes for high‐altitude adaptation. In the future, more studies should be focused on speciation and adaptation mechanisms of the alpine species in the QTPsl based on the cutting‐edge methods.

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“…Natural hybridization is frequent in plants and plays a crucial role in the formation and maintenance of species. In recent decades, natural hybridization has been well-documented for numerous herbaceous (e.g., Helianthus [ 1 , 2 ], Iris [ 3 ], Senecio [ 4 ], Viola [ 5 ], Gagea [ 6 ], Brassica [ 7 ], Mimulus [ 8 ]) and some woody plant taxa (e.g., Pinus [ 9 , 10 ], Ostryopsis [ 11 , 12 ], Rhododendron [ 13 – 16 ]). For the most part, studies reveal that when two or more closely related species are in sympatry, hybridization frequently occurs and natural hybrid zones are likely to form (e.g.…”

Section: Introductionmentioning

confidence: 99%

Natural hybridization among three Rhododendron species (Ericaceae) revealed by morphological and genomic evidence

et al. 2021

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Background Natural hybridization can influence the adaptive response to selection and accelerate species diversification. Understanding the composition and structure of hybrid zones may elucidate patterns of hybridization processes that are important to the formation and maintenance of species, especially for taxa that have experienced rapidly adaptive radiation. Here, we used morphological traits, ddRAD-seq and plastid DNA sequence data to investigate the structure of a Rhododendron hybrid zone and uncover the hybridization patterns among three sympatric and closely related species. Results Our results show that the hybrid zone is complex, where bi-directional hybridization takes place among the three sympatric parental species: R. spinuliferum, R. scabrifolium, and R. spiciferum. Hybrids between R. spinuliferum and R. spiciferum (R. ×duclouxii) comprise multiple hybrid classes and a high proportion of F1 generation hybrids, while a novel hybrid taxon between R. spinuliferum and R. scabrifolium dominated the F2 generation, but no backcross individuals were detected. The hybrid zone showed basically coincident patterns of population structure between genomic and morphological data. Conclusions Natural hybridization exists among the three Rhododendron species in the hybrid zone, although patterns of hybrid formation vary between hybrid taxa, which may result in different evolutionary outcomes. This study represents a unique opportunity to dissect the ecological and evolutionary mechanisms associated with adaptive radiation of Rhododendron species in a biodiversity hotspot.

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Hybrid speciation via inheritance of alternate alleles of parental isolating genes

Cited by 78 publications

References 87 publications

Genomic analyses overturn two long‐standing homoploid hybrid speciation hypotheses

Genomic analyses overturn two long‐standing homoploid hybrid speciation hypotheses

Evolutionary origin of species diversity on the Qinghai–Tibet Plateau

Natural hybridization among three Rhododendron species (Ericaceae) revealed by morphological and genomic evidence

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