On the importance of balancing selection in plants

This is the peer reviewed version of the following article: Delph, L. F. and Kelly, J. K. (2014), On the importance of balancing selection in plants. New Phytol, 201: 45–56. doi:10.1111/nph.12441, which has been published in final form at http://doi.org/10.1111/nph.12441. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.Balancing selection refers to a variety of selective regimes that maintain advantageous genetic diversity within populations. We review the history of the ideas regarding the types of selection that maintain such polymorphism in flowering plants, notably heterozygote advantage, negative frequency-dependent selection, and spatial heterogeneity. One shared feature of these mechanisms is that whether an allele is beneficial or detrimental is conditional on its frequency in the population. We highlight examples of balancing selection on a variety of discrete traits. These include the well-referenced case of self-incompatibility and recent evidence from species with nuclear-cytoplasmic gynodioecy, both of which exhibit trans-specific polymorphism, a hallmark of balancing selection. We also discuss and give examples of how spatial heterogeneity in particular, which is often thought unlikely to allow protected polymorphism, can maintain genetic variation in plants (which are rooted in place) as a result of microhabitat selection. Lastly, we discuss limitations of the protected polymorphism concept for quantitative traits, where selection can inflate the genetic variance without maintaining specific alleles indefinitely. We conclude that while discrete-morph variation provides the most unambiguous cases of protected polymorphism, they represent only a fraction of the balancing selection at work in plants

Factors affecting relative seed fitness and female frequency in a gynodioecious species, Silene acaulis

ABSTRACT Sex-ratio variation is common among gynodioecious species. One argument predicts that when sex is determined by a combination of nuclear and cytoplasmic factors, the frequency of females will be determined by genetic rather than ecological factors. An alternative argument suggests that the relative seed fitness of the female and hermaphroditic morphs will control female frequency. Hence, sex-ratio variation can be influenced by any factor that affects relative seed fitness, including ecological factors such as variation in pollination or site quality. In this study, we investigated sex-ratio variation in the gynodioecious species Silene acaulis, which has nuclear-cytoplasmic sex determination. We determined whether the frequency of females in 10 sites on Niwot Ridge, in the Front Range of Colorado, was correlated with the quality of the site or the relative seed fitness of the two morphs. Furthermore, we determined whether the two morphs differed consistently in investment in flowers, ovules, seeds and fruits. We found significant variation in sex ratio, site quality and relative seed fitness of the two morphs across sites. Although ovule number was greater in flowers on females, seed number per fruit did not vary in a consistent manner between morphs. The morphs differed consistently only in their propensity to produce fruit, with hermaphrodites exhibiting highly variable, and relatively low, fruit set compared to females. Female frequency was not significantly correlated with site quality. However, the relative seed fitness of the morphs was significantly correlated with site quality and the frequency of females. These results suggest that ecological factors do play a role in determining female frequency in S. acaulis and, consequently, can impact breeding-system evolution in this long-lived species

Sex-specific natural selection on SNPs in Silene latifolia

Selection that acts in a sex-specific manner causes the evolution of sexual dimorphism. Sex-specific phenotypic selection has been demonstrated in many taxa and can be in the same direction in the two sexes (differing only in magnitude), limited to one sex, or in opposing directions (antagonistic). Attempts to detect the signal of sex-specific selection from genomic data have confronted numerous difficulties. These challenges highlight the utility of “direct approaches,” in which fitness is predicted from individual genotype within each sex. Here, we directly measured selection on Single Nucleotide Polymorphisms (SNPs) in a natural population of the sexually dimorphic, dioecious plant, Silene latifolia. We measured flowering phenotypes, estimated fitness over one reproductive season, as well as survival to the next year, and genotyped all adults and a subset of their offspring for SNPs across the genome. We found that while phenotypic selection was congruent (fitness covaried similarly with flowering traits in both sexes), SNPs showed clear evidence for sex-specific selection. SNP-level selection was particularly strong in males and may involve an important gametic component (e.g., pollen competition). While the most significant SNPs under selection in males differed from those under selection in females, paternity selection showed a highly polygenic tradeoff with female survival. Alleles that increased male mating success tended to reduce female survival, indicating sexual antagonism at the genomic level. Perhaps most importantly, this experiment demonstrates that selection within natural populations can be strong enough to measure sex-specific fitness effects of individual loci

Genetically based population divergence of Silene latifolia from two climate regions

ABSTRACT Background: Plants in hot and dry climates often flower earlier, make thicker leaves, and produce fewer flowers than conspecifics from relatively wet, cool climates. Silene latifolia, a dioecious, short-lived, flowering perennial, grows in both of these climates in Europe. Question: Is variation in traits seen among populations with divergent climates a result of genetic changes in response to local environmental conditions, differences in the degree of sexual dimorphism, or phenotypic plasticity? Hypothesis: Traits will differ between populations in a common garden as a result of genetic divergence, and exhibit a pattern of variation that is congruent with adaptation to climate. Methods: Morphological and phenological measurements were taken during two flowering seasons on plants growing in Croatia (relatively wet and cool) and Spain (hot and dry). Seeds from both regions were grown to flowering in the greenhouse and several traits were measured. Results: Significant divergence in traits existed between Croatia and Spain that persisted in the common garden (greenhouse), indicating that populations in these two regions likely represent different ecotypes. Plants from Spain flowered earlier in the field, made thicker leaves, and produced fewer flowers than plants from Croatia. Plants from Spain also showed greater sexual dimorphism than those from Croatia

Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants

<p>Abstract</p> <p>Background</p> <p>It has long been known that rates of synonymous substitutions are unusually low in mitochondrial genes of flowering and other land plants. Although two dramatic exceptions to this pattern have recently been reported, it is unclear how often major increases in substitution rates occur during plant mitochondrial evolution and what the overall magnitude of substitution rate variation is across plants.</p> <p>Results</p> <p>A broad survey was undertaken to evaluate synonymous substitution rates in mitochondrial genes of angiosperms and gymnosperms. Although most taxa conform to the generality that plant mitochondrial sequences evolve slowly, additional cases of highly accelerated rates were found. We explore in detail one of these new cases, within the genus <it>Silene</it>. A roughly 100-fold increase in synonymous substitution rate is estimated to have taken place within the last 5 million years and involves only one of ten species of <it>Silene </it>sampled in this study. Examples of unusually slow sequence evolution were also identified. Comparison of the fastest and slowest lineages shows that synonymous substitution rates vary by four orders of magnitude across seed plants. In other words, some plant mitochondrial lineages accumulate more synonymous change in 10,000 years than do others in 100 million years. Several perplexing cases of gene-to-gene variation in sequence divergence within a plant were uncovered. Some of these probably reflect interesting biological phenomena, such as horizontal gene transfer, mitochondrial-to-nucleus transfer, and intragenomic variation in mitochondrial substitution rates, whereas others are likely the result of various kinds of errors.</p> <p>Conclusion</p> <p>The extremes of synonymous substitution rates measured here constitute by far the largest known range of rate variation for any group of organisms. These results highlight the utility of examining absolute substitution rates in a phylogenetic context rather than by traditional pairwise methods. Why substitution rates are generally so low in plant mitochondrial genomes yet occasionally increase dramatically remains mysterious.</p

Herbivore-mediated negative frequency-dependent selection underlies a trichome dimorphism in nature

Authors are grateful for funding provided by an NSF GRFP to J.K.G. (2015195769) and DEB‐1353970 to L.F.D.Negative frequency‐dependent selection (NFDS) has been shown to maintain polymorphism in a diverse array of traits. The action of NFDS has been confirmed through modeling, experimental approaches, and genetic analyses. In this study, we investigated NFDS in the wild using morph‐frequency changes spanning a 20‐year period from over 30 dimorphic populations of Datura wrightii. In these populations, plants either possess glandular (sticky) or non‐glandular (velvety) trichomes, and the ratio of these morphs varies substantially among populations. Our method provided evidence that NFDS, rather than drift or migration, is the primary force maintaining this dimorphism. Most populations that were initially dimorphic remained dimorphic, and the overall mean and variance in morph frequency did not change over time. Furthermore, morph‐frequency differences were not related to geographic distances. Together, these results indicate that neither directional selection, drift, or migration played a substantial role in determining morph frequencies. However, as predicted by negative frequency‐dependent selection, we found that the rare morph tended to increase in frequency, leading to a negative relationship between the change in the frequency of the sticky morph and its initial frequency. In addition, we found that morph‐frequency change over time was significantly correlated with the damage inflicted by two herbivores: Lema daturaphila and Tupiochoris notatus. The latter is a specialist on the sticky morph and damage by this herbivore was greatest when the sticky morph was common. The reverse was true for L. daturaphila, such that damage increased with the frequency of the velvety morph. These findings suggest that these herbivores contribute to balancing selection on the observed trichome dimorphism.Publisher PDFPeer reviewe

X Linkage of AP3A, a Homolog of the Y-Linked MADS-Box Gene AP3Y in Silene latifolia and S. dioica

Background: The duplication of autosomal genes onto the Y chromosome may be an important element in the evolution of sexual dimorphism.A previous cytological study reported on a putative example of such a duplication event in a dioecious tribe of Silene (Caryophyllaceae): it was inferred that the Y-linked MADS-box gene AP3Y originated from a duplication of the reportedly autosomal orthologAP3A. However, a recent study, also using cytological methods, indicated that AP3A is X-linked in Silenelatifolia. Methodology/Principal Findings: In this study, we hybridized S. latifolia and S. dioicato investigate whether the pattern of X linkage is consistent among distinct populations, occurs in both species, and is robust to genetic methods. We found inheritance patterns indicative of X linkage of AP3A in widely distributed populations of both species. Conclusions/Significance: X linkage ofAP3A and Y linkage of AP3Yin both species indicates that the genes ’ ancestral progenitor resided on the autosomes that gave rise to the sex chromosomesand that neither gene has moved between chromosomes since species divergence.Consequently, our results do not support the contention that inter-chromosomal gene transfer occurred in the evolution of SlAP3Y from SlAP3A