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Ancient DNA reveals the timing and persistence of organellar genetic bottlenecks over 3,000 years of sunflower domestication and improvement

Wales, Nathan, Akman, Melis, Watson, Ray H. B., Sánchez Barreiro, Fátima, Smith, Bruce D., Gremillion, Kristen J., Gilbert, M. Thomas P., Blackman, Benjamin K.·2019·Evolutionary Applications
DOI 10.1111/eva.12594PMC PMC6304678
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Abstract

Here, we report a comprehensive paleogenomic study of archaeological and ethnographic sunflower remains that provides significant new insights into the process of domestication of this important crop.DNA from both ancient and historic contexts yielded high proportions of endogenous DNA, and although archaeological DNA was found to be highly degraded, it still provided sufficient coverage to analyze genetic changes over time. Shotgun sequencing data from specimens from the Eden's Bluff archaeological site in Arkansas yielded organellar DNA sequence from specimens up to 3,100 years old. Their sequences match those of modern cultivated sunflowers and are consistent with an early domestication bottleneck in this species. Our findings also suggest that recent breeding of sunflowers has led to a loss of genetic diversity that was present only a century ago in Native American landraces. These breeding episodes also left a profound signature on the mitochondrial and plastid haplotypes in cultivars, as two types were intentionally introduced from other Helianthus species for crop improvement. These findings gained from ancient and historic sunflower specimens underscore how future in‐depth gene‐based analyses can advance our understanding of the pace and targets of selection during the domestication of sunflower and other crop species.

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Figure 1 Map of sampling locations and archaeological sites. Ethnographic samples (and number of accessions sampled) are in red, and landraces are in blue. Archaeological sites with ancient sunflower material discussed in the text are marked by yellow circles. Eden's Bluff, the site from which all archaeological remains detailed in this article were sampled, is bolded
Figure 1 Map of sampling locations and archaeological sites. Ethnographic samples (and number of accessions sampled) are in red, and landraces are in blue. Archaeological sites with ancient sunflower material discussed in the text are marked by yellow circles. Eden's Bluff, the site from which all archaeological remains detailed in this article were sampled, is boldedCC BY · PubMed Central
Figure 2 DNA content of ancient and ethnographic landrace samples and extraction controls. Percentage of total reads mapping to the sunflower genome and relative proportion of unmapped reads assigned to kingdom‐level taxa based on a random sampling of 10,000 unmapped reads
Figure 2 DNA content of ancient and ethnographic landrace samples and extraction controls. Percentage of total reads mapping to the sunflower genome and relative proportion of unmapped reads assigned to kingdom‐level taxa based on a random sampling of 10,000 unmapped readsCC BY · PubMed Central
Figure 3 Plastome haplotype networks constructed with wild, cultivated, landrace, ethnographic, and archaeological sunflowers (a), and plastome haplotype network constructed without the archaeological sunflowers (b). The size of the circles corresponds to number of individuals present, and the number of polymorphic sites between individual haplotypes is indicated by tick marks. Haplotype classes for each sample are included in Table S3. Class 1 is a core domestication haplotype and is composed of wild Helianthus annuus, archaeological specimens, ethnographic samples, extant landraces, and modern cultivars. Class 2 also represents a haplotype that entered the domestication process thousands of years ago; however, it is not observed in cultivars. Class 3 consists of R‐type elite cultivars used in hybrid breeding, and was presumably introduced into domesticated germplasm from H. petiolaris in the 20th century; as discussed in the text, we suspect two Mexican landraces in Class 3 may originate from misidentified cultivars. Class 4 consists exclusively of elite cultivars, and was likely introduced from crop wild relatives, putatively H. argophyllus, during recent breeding for resistance to pathogens and diseases
Figure 3 Plastome haplotype networks constructed with wild, cultivated, landrace, ethnographic, and archaeological sunflowers (a), and plastome haplotype network constructed without the archaeological sunflowers (b). The size of the circles corresponds to number of individuals present, and the number of polymorphic sites between individual haplotypes is indicated by tick marks. Haplotype classes for each sample are included in Table S3. Class 1 is a core domestication haplotype and is composed of wild Helianthus annuus, archaeological specimens, ethnographic samples, extant landraces, and modern cultivars. Class 2 also represents a haplotype that entered the domestication process thousands of years ago; however, it is not observed in cultivars. Class 3 consists of R‐type elite cultivars used in hybrid breeding, and was presumably introduced into domesticated germplasm from H. petiolaris in the 20th century; as discussed in the text, we suspect two Mexican landraces in Class 3 may originate from misidentified cultivars. Class 4 consists exclusively of elite cultivars, and was likely introduced from crop wild relatives, putatively H. argophyllus, during recent breeding for resistance to pathogens and diseasesCC BY · PubMed Central
Figure 4 Mitochondrial haplotype network constructed with wild, cultivated, landrace and ethnographic sunflowers. The size of the circles corresponds to number of individuals present, and the number of polymorphic sites between individual haplotypes is indicated by tick marks. Haplotype classes for each sample are included in Table S3. Class 1 is composed of individuals sharing the same haplotype and also those that diverge by only one or two polymorphic sites. Due to uniparental inheritance of organelles, the mitochondrial classes contain the same individuals as the plastome classes. See Figure 3 for information on the domestication haplotypes (Classes 1 and 2) and those introduced to modern cultivars during 20th‐century breeding (Classes 3 and 4)
Figure 4 Mitochondrial haplotype network constructed with wild, cultivated, landrace and ethnographic sunflowers. The size of the circles corresponds to number of individuals present, and the number of polymorphic sites between individual haplotypes is indicated by tick marks. Haplotype classes for each sample are included in Table S3. Class 1 is composed of individuals sharing the same haplotype and also those that diverge by only one or two polymorphic sites. Due to uniparental inheritance of organelles, the mitochondrial classes contain the same individuals as the plastome classes. See Figure 3 for information on the domestication haplotypes (Classes 1 and 2) and those introduced to modern cultivars during 20th‐century breeding (Classes 3 and 4)CC BY · PubMed Central

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    Orlando, L., Allaby, R., Skoglund, P., Der Sarkissian, C., Stockhammer, P. W., Ávila-Arcos, M. C., Fu, Q., Krause, J., Willerslev, E., Stone, A. C., et al. (2021) · Nature Reviews Methods Primers · doi:10.1038/s43586-020-00011-0 · Cited by 411

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Metadata

Authors
Wales, N., Akman, M., Watson, R. H. B., Sánchez Barreiro, F., Smith, B. D., Gremillion, K. J., Gilbert, M. T. P., & Blackman, B. K.
Affiliations
  • Department of Plant and Microbial Biology University of California Berkeley CA USA
  • Centre for GeoGenetics Natural History Museum of Denmark University of Copenhagen Copenhagen Denmark
  • The Santa Fe Institute Santa Fe NM USA
  • Department of Anthropology Ohio State University Columbus OH USA
ORCID
Wales, Nathan
Venue
Evolutionary Applications
Publisher
Wiley
Published
2018-02-13
Volume
12
Issue
1
Pages
38-53
ISSN
1752-4571
DOI
10.1111/eva.12594
PMC
PMC6304678
Cited by
35
References
5
Language
en
Licence
Funders
  • National Science Foundation (1354622, 1640788)
  • Danmarks Grundforskningsfond

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