Divergent natural selection promotes local adaptation and can lead to reproductive isolation of populations in contrasting environments; however, the genetic basis of local adaptation remains largely ...unresolved in natural populations. Local adaptation might result from antagonistic pleiotropy, where alternate alleles are favoured in distinct habitats, and polymorphism is maintained by selection. Alternatively, under conditional neutrality some alleles may be favoured in one environment but neutral at other locations. Antagonistic pleiotropy maintains genetic variation across the landscape; however, there is a systematic bias against discovery of antagonistic pleiotropy because the fitness benefits of local alleles need to be significant in at least two environments. Here, we develop a generally applicable method to investigate polygenic local adaptation and identify loci that are the targets of selection. This approach evaluates allele frequency changes after selection at loci across the genome to distinguish antagonistic pleiotropy from conditional neutrality and deleterious variation. We investigate local adaptation at the qualitative trait loci (QTL) level in field experiments, in which we expose 177 F6 recombinant inbred lines and parental lines of Boechera stricta (Brassicaceae) to their parental environments over two seasons. We demonstrate polygenic selection for native alleles in both environments, with 2.8% of the genome exhibiting antagonistic pleiotropy and 8% displaying conditional neutrality. Our study strongly supports antagonistic pleiotropy at one large‐effect flowering phenology QTL (nFT): native homozygotes had significantly greater probabilities of flowering than foreign homozygotes in both parental environments. Such large‐scale field studies are essential to elucidate the genetic basis of adaptation in natural populations.
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When two species meet in secondary contact, the production of low fitness hybrids may be prevented by the adaptive evolution of increased prezygotic isolation, a process known as reinforcement. ...Theoretical challenges to the evolution of reinforcement are generally cast as a coordination problem, i.e., “how can statistical associations between traits and preferences be maintained in the face of recombination?” However, the evolution of reinforcement also poses a potential conflict between mates. For example, the opportunity costs to hybridization may differ between the sexes or species. This is particularly likely for reinforcement based on postmating prezygotic (PMPZ) incompatibilities, as the ability to fertilize both conspecific and heterospecific eggs is beneficial to male gametes, but heterospecific mating may incur a cost for female gametes. We develop a population genetic model of interspecific conflict over reinforcement inspired by “gametophytic factors”, which act as PMPZ barriers among
Zea mays
subspecies. We demonstrate that this conflict results in the transient evolution of reinforcement—after females adaptively evolve to reject gametes lacking a signal common in conspecific gametes, this gamete signal adaptively introgresses into the other population. Ultimately, the male gamete signal fixes in both species, and isolation returns to pre-reinforcement levels. We interpret geographic patterns of isolation among
Z
.
mays
subspecies considering these findings and suggest when and how this conflict can be resolved. Our results suggest that sexual conflict over fertilization may pose an understudied obstacle to the evolution of reinforcement.
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Despite decades of research, the evolution of sex remains an enigma in evolutionary biology. Typically, research addresses the costs of sex and asexuality to characterize the circumstances favoring ...one reproductive mode. Surprisingly few studies address the influence of common traits that are, in many organisms, obligately correlated with asexuality, including hybridization and polyploidy. These characteristics have substantial impacts on traits under selection. In particular, the fitness consequences of hybridization (i.e., reduced fitness due to interspecific reproductive isolation) will influence the evolution of sex. This may comprise a cost of either sex or asexuality due to the link between hybridity and asexuality. We examined reproductive isolation in the formation of de novo hybrid lineages between 2 widespread species in the ecological model system Boechera. Seventeen percent of 664 crosses produced F1 fruits, and only 10% of these were viable, suggesting that postmating prezygotic and postzygotic barriers inhibit hybrid success in this system. The postmating prezygotic barrier was asymmetrical, with 110 of 115 total F1 fruits produced when Boechera stricta acted as maternal parent. This asymmetry was confirmed in wild-collected lineages, using a chloroplast phylogeny of wild-collected B. stricta, Boechera retrofracta, and hybrids. We next compared fitness of F2 hybrids and selfed parental B. stricta lines, finding that F2 fitness was reduced by substantial hybrid sterility. Multiple reproductively isolating barriers influence the formation and fitness of hybrid lineages in the wild, and the costs of hybridization likely have profound impacts on the evolution of sex in the natural environment.
The Boechera model system for evolutionary ecology Rushworth, Catherine A.; Wagner, Maggie R.; Mitchell‐Olds, Thomas ...
American journal of botany,
November 2022, 2022-11-00, 20221101, Volume:
109, Issue:
11
Journal Article
Peer reviewed
Open access
Model systems in biology expand the research capacity of individuals and the community. Closely related to Arabidopsis, the genus Boechera has emerged as an important ecological model owing to the ...ability to integrate across molecular, functional, and eco‐evolutionary approaches. Boechera species are broadly distributed in relatively undisturbed habitats predominantly in western North America and provide one of the few experimental systems for identification of ecologically important genes through genome‐wide association studies and investigations of selection with plants in their native habitats. The ecologically, evolutionarily, and agriculturally important trait of apomixis (asexual reproduction via seeds) is common in the genus, and field experiments suggest that abiotic and biotic environments shape the evolution of sex. To date, population genetic studies have focused on the widespread species B. stricta, detailing population divergence and demographic history. Molecular and ecological studies show that balancing selection maintains genetic variation in ~10% of the genome, and ecological trade‐offs contribute to complex trait variation for herbivore resistance, flowering phenology, and drought tolerance. Microbiome analyses have shown that host genotypes influence leaf and root microbiome composition, and the soil microbiome influences flowering phenology and natural selection. Furthermore, Boechera offers numerous opportunities for investigating biological responses to global change. In B. stricta, climate change has induced a shift of >2 weeks in the timing of first flowering since the 1970s, altered patterns of natural selection, generated maladaptation in previously locally‐adapted populations, and disrupted life history trade‐offs. Here we review resources and results for this eco‐evolutionary model system and discuss future research directions.
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Scientific societies have the potential to catalyze support for communities that have been historically excluded from science. Many of these societies have formed committees to propose and administer ...initiatives to promote the career and well-being of their members, with a special emphasis on racial and ethnic minorities. Yet, these societies are rarely armed with data to inform their proposals. Three of the evolution societies (American Society of Naturalists, “ASN”; Society of Systematic Biologists, “SSB”; Society for the Study of Evolution, “SSE”) have also formed Diversity, Equity, and Inclusion committees in the last few years. As a first step in determining the needs of the societies, these committees collected data on the demographic characteristics of the societies’ constituents by surveying the attendants of the Evolution 2019 meeting. Here, we report the proportions for different demographic groups in attendance at the meeting and compare these proportions to the demographics of recipients of Ph.D. degrees either in evolutionary biology or in the broader life sciences, as well as population demographics of the USA. Our results indicate that historically excluded groups are still underrepresented across US-based evolutionary biology professional societies. We explore whether demographic composition differs at different professional stages and find that representation for women and LGBTQ+ members decreases as the career stage progresses. We also find some evidence for heterogeneity across societies in terms of racial composition. Finally, we discuss the caveats and limitations of our procedures. Our results will serve to inform future efforts to collect demographic data at the society levels, which should in turn be used to design and implement evidence-based initiatives for inclusion and equity. This report should be a starting point for systematic efforts to characterize the ever-changing representation in evolutionary biology and to work toward the inclusion of all groups.
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The Ecology of Hybrid Incompatibilities Thompson, Ken A; Brandvain, Yaniv; Coughlan, Jenn M ...
Cold Spring Harbor perspectives in biology,
2023-Dec-27, 2023-12-27, 20231227
Journal Article
Peer reviewed
Ecologically mediated selection against hybrids, caused by hybrid phenotypes fitting poorly into available niches, is typically viewed as distinct from selection caused by epistatic Dobzhansky-Muller ...hybrid incompatibilities. Here, we show how selection against transgressive phenotypes in hybrids manifests as incompatibility. After outlining our logic, we summarize current approaches for studying ecology-based selection on hybrids. We then quantitatively review QTL-mapping studies and find traits differing between parent taxa are typically polygenic. Next, we describe how verbal models of selection on hybrids translate to phenotypic and genetic fitness landscapes, highlighting emerging approaches for detecting polygenic incompatibilities. Finally, in a synthesis of published data, we report that trait transgression-and thus possibly extrinsic hybrid incompatibility in hybrids-escalates with the phenotypic divergence between parents. We discuss conceptual implications and conclude that studying the ecological basis of hybrid incompatibility will facilitate new discoveries about mechanisms of speciation.
Premise of the Study
Ecological differentiation (ED) between sexual and asexual organisms may permit the maintenance of reproductive polymorphism. Several studies of sexual/asexual ED in plants have ...shown that the geographic ranges of asexuals extend beyond those of sexuals, often in areas of higher latitude or elevation. But very little is known about ED at fine scales, wherein coexistence of sexuals and asexuals may be permitted by differential niche occupation.
Methods
We used 149 populations of sexual and apomictic lineages in the genus Boechera (rock cress) collected across a portion of this mustard's vast range. We characterized reproductive mode, ploidy, and species identity or hybrid parentage of each individual, and then used a multipronged statistical approach to (1) identify ED between sexuals and asexuals; (2) investigate the impacts of two confounding factors, polyploidy and hybridization, on ED; and (3) determine the environmental variables underlying ED.
Key Results
We found that sexuals and asexuals are significantly ecologically differentiated across the landscape, despite fine‐scale interdigitation of these two reproductive forms. Asexual reproduction was strongly associated with greater disturbance, reduced slope, and greater environmental variability. Although ploidy had little effect on the patterns observed, hybridization has a unique impact on the relationships between asexual reproduction and specific environmental variables.
Conclusions
Ecological differentiation along the axes of disturbance, slope, and climatic variability, as well as the effects of heterozygosity, may contribute to the maintenance of sexuality and asexuality across the landscape, ultimately impacting the establishment and spread of asexual lineages.
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Angiosperm phylogeny: 17 genes, 640 taxa Soltis, Douglas E.; Smith, Stephen A.; Cellinese, Nico ...
American journal of botany,
April 2011, Volume:
98, Issue:
4
Journal Article
Peer reviewed
Open access
Premise of the study. Recent analyses employing up to five genes have provided numerous insights into angiosperm phylogeny, but many relationships have remained unresolved or poorly supported. In the ...hope of improving our understanding of angiosperm phylogeny, we expanded sampling of taxa and genes beyond previous analyses. Methods: We conducted two primary analyses based on 640 species representing 330 families. The first included 25260 aligned base pairs (bp) from 17 genes (representing all three plant genomes, i. e., nucleus, plastid, and mitochondrion). The second included 19846 aligned bp from 13 genes (representing only the nucleus and plastid). Key results: Many important questions of deep-level relationships in the nonmonocot angiosperms have now been resolved with strong support. Amborellaceae, Nymphaeales, and Austrobaileyales are successive sisters to the remaining angiosperms (Mesangiospermae), which are resolved into Chloranthales + Magnoliidae as sister to Monocotyledoneae + Ceratophyllaceae + Eudicotyledoneae. Eudicotyledoneae contains a basal grade subtending Gunneridae. Within Gunneridae, Gunnerales are sister to the remainder (Pentapetalae), which comprises (1) Superrosidae, consisting of Rosidae (including Vitaceae) and Saxifragales; and (2) Superasteridae, comprising Berberidopsidales, Santalales, CaryophyHales, Asteridae, and, based on this study, Dilleniaceae (although other recent analyses disagree with this placement). Within the major subclades of Pentapetalae, most deep-level relationships are resolved with strong support. Conclusions: Our analyses confirm that with large amounts of sequence data, most deep-level relationships within the angiosperms can be resolved. We anticipate that this well-resolved angiosperm tree will be of broad utility for many areas of biology, including physiology, ecology, paleobiology, and genomics.
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The selection and development of a study system for evolutionary and ecological functional genomics (EEFG) depend on a variety of factors. Here, we present the genus Boechera as an exemplary system ...with which to address ecological and evolutionary questions. Our focus on Boechera is based on several characteristics as follows: (i) native populations in undisturbed habitats where current environments reflect historical conditions over several thousand years; (ii) functional genomics benefitting from its close relationship to Arabidopsis thaliana; (iii) inbreeding tolerance enabling development of recombinant inbred lines, near‐isogenic lines and positional cloning; (iv) interspecific crosses permitting mapping for genetic analysis of speciation; (v) apomixis (asexual reproduction by seeds) in a genetically tractable diploid; and (vi) broad geographic distribution in North America, permitting ecological genetics for a large research community. These characteristics, along with the current sequencing of three Boechera species by the Joint Genome Institute, position Boechera as a rapidly advancing system for EEFG studies.
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Premise
The ability to sequence genome‐scale data from herbarium specimens would allow for the economical development of data sets with broad taxonomic and geographic sampling that would otherwise ...not be possible. Here, we evaluate the utility of a basic double‐digest restriction site–associated DNA sequencing (ddRADseq) protocol using DNAs from four genera extracted from both silica‐dried and herbarium tissue.
Methods
DNAs from Draba, Boechera, Solidago, and Ilex were processed with a ddRADseq protocol. The effects of DNA degradation, taxon, and specimen age were assessed.
Results
Although taxon, preservation method, and specimen age affected data recovery, large phylogenetically informative data sets were obtained from the majority of samples.
Discussion
These results suggest that herbarium samples can be incorporated into ddRADseq project designs, and that specimen age can be used as a rapid on‐site guide for sample choice. The detailed protocol we provide will allow users to pursue herbarium‐based ddRADseq projects that minimize the expenses associated with fieldwork and sample evaluation.
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