Population genomics of parallel hybrid zones in the mimetic butterflies,H. melpomeneandH. erato

Hybrid zones can be valuable tools for studying evolution and identifying genomic regions responsible for adaptive divergence and underlying phenotypic variation. Hybrid zones between subspecies of Heliconius butterflies can be very narrow and are maintained by strong selection acting on colour pattern. The co-mimetic species H. erato and H. melpomene have parallel hybrid zones where both species undergo a change from one colour pattern form to another. We use restriction associated DNA sequencing to obtain several thousand genome wide sequence markers and use these to analyse patterns of population divergence across two pairs of parallel hybrid zones in Peru and Ecuador. We compare two approaches for analysis of this type of data; alignment to a reference genome and de novo assembly, and find that alignment gives the best results for species both closely (H. melpomene) and distantly (H. erato, ~15% divergent) related to the reference sequence. Our results confirm that the colour pattern controlling loci account for the majority of divergent regions across the genome, but we also detect other divergent regions apparently unlinked to colour pattern differences. We also use association mapping to identify previously unmapped colour pattern loci, in particular the Ro locus. Finally, we identify within our sample a new cryptic population of H. timareta in Ecuador, which occurs at relatively low altitude and is mimetic with H. melpomene malleti.

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Site-specific genetic divergence in parallel hybrid zones suggests nonallopatric evolution of reproductive barriers

Molecular Ecology ◽

10.1111/j.1365-294x.2006.03067.x ◽

2006 ◽

Vol 15 (13) ◽

pp. 4021-4031 ◽

Cited By ~ 299

Author(s):

M. PANOVA ◽

J. HOLLANDER ◽

K. JOHANNESSON

Keyword(s):

Genetic Divergence ◽

Hybrid Zones ◽

Reproductive Barriers ◽

Site Specific ◽

Parallel Hybrid

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Natural selection maintains species despite widespread hybridization in the desert shrub Encelia

10.1101/2020.01.23.917021 ◽

2020 ◽

Cited By ~ 1

Author(s):

Christopher D DiVittorio ◽

Sonal Singhal ◽

Adam B Roddy ◽

Felipe Zapata ◽

David D Ackerly ◽

...

Keyword(s):

Gene Flow ◽

Natural Selection ◽

Field Experiments ◽

Population Genomics ◽

Coastal Dunes ◽

Species Boundaries ◽

Hybrid Zones ◽

Desert Shrubs ◽

Species Complexes ◽

Species Pairs

ABSTRACTNatural selection is an important driver of genetic and phenotypic differentiation between species. A powerful way to test the role of natural selection in the formation and maintenance of species is to study species complexes in which potential gene flow is high but realized gene flow is low. For a recent radiation of New World desert shrubs (Encelia: Asteraceae), we use fine-scale geographic sampling and population genomics to determine patterns of gene flow across two hybrid zones formed between two independent pairs of species with parapatric distributions. After finding evidence for extremely strong selection at both hybrid zones, we use a combination of field experiments, high-resolution imaging, and physiological measurements to determine the ecological basis for selection at one of the hybrid zones. Our results identify multiple ecological mechanisms of selection (drought, salinity, herbivory, and burial) that together are sufficient to maintain species boundaries despite high rates of hybridization. Given that multiple pairs of species hybridize at ecologically divergent parapatric boundaries in the adaptive radiation of Encelia, such mechanisms may maintain species boundaries throughout this group.SIGNIFICANCE STATEMENTIn Baja California, the deserts meet the coastal dunes in a narrow transition visible even from satellite images. We study two species pairs of desert shrubs (Encelia) that occur across this transition. Although these species can interbreed, they remain distinct. Using a combination of genetics, field experiments, 3D-imaging, and physiological measurements, we show that natural selection counteracts the homogenizing effects of gene exchange. The different habitats of these species create multiple mechanisms of selection - drought, salinity, herbivory, and burial, which together maintain these species in their native habitats and their hybrids in intermediate habitats. This study illustrates how environmental factors influence traits and fitness and how this in turn maintain species, highlighting the importance of natural selection in speciation.

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Natural selection maintains species despite frequent hybridization in the desert shrub Encelia

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2001337117 ◽

2020 ◽

Vol 117 (52) ◽

pp. 33373-33383

Author(s):

Christopher T. DiVittorio ◽

Sonal Singhal ◽

Adam B. Roddy ◽

Felipe Zapata ◽

David D. Ackerly ◽

...

Keyword(s):

Gene Flow ◽

Natural Selection ◽

Field Experiments ◽

Population Genomics ◽

Species Boundaries ◽

Hybrid Zones ◽

Phenotypic Differentiation ◽

Desert Shrubs ◽

Resolution Imaging ◽

Ecological Mechanisms

Natural selection is an important driver of genetic and phenotypic differentiation between species. For species in which potential gene flow is high but realized gene flow is low, adaptation via natural selection may be a particularly important force maintaining species. For a recent radiation of New World desert shrubs (Encelia: Asteraceae), we use fine-scale geographic sampling and population genomics to determine patterns of gene flow across two hybrid zones formed between two independent pairs of species with parapatric distributions. After finding evidence for extremely strong selection at both hybrid zones, we use a combination of field experiments, high-resolution imaging, and physiological measurements to determine the ecological basis for selection at one of the hybrid zones. Our results identify multiple ecological mechanisms of selection (drought, salinity, herbivory, and burial) that together are sufficient to maintain species boundaries despite high rates of hybridization. Given that multiple pairs of Encelia species hybridize at ecologically divergent parapatric boundaries, such mechanisms may maintain species boundaries throughout Encelia.

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