Global urban environmental change drives adaptation in white clover

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale

Gene duplicates cause hybrid lethality between sympatric species of <i>Mimulus</i>

<div><p>Hybrid incompatibilities play a critical role in the evolution and maintenance of species. We have discovered a simple genetic incompatibility that causes lethality in hybrids between two closely related species of yellow monkeyflower (<i>Mimulus guttatus</i> and <i>M</i>. <i>nasutus</i>). This hybrid incompatibility, which causes one sixteenth of F₂ hybrid seedlings to lack chlorophyll and die shortly after germination, occurs between sympatric populations that are connected by ongoing interspecific gene flow. Using complimentary genetic mapping and gene expression analyses, we show that lethality occurs in hybrids that lack a functional copy of the critical photosynthetic gene <i>pTAC14</i>. In <i>M</i>. <i>guttatus</i>, this gene was duplicated, but the ancestral copy is no longer expressed. In <i>M</i>. <i>nasutus</i>, the duplication is missing altogether. As a result, hybrids die when they are homozygous for the nonfunctional <i>M</i>. <i>guttatus</i> copy and missing the duplicate from <i>M</i>. <i>nasutus</i>, apparently due to misregulated transcription of key photosynthetic genes. Our study indicates that neutral evolutionary processes may play an important role in the evolution of hybrid incompatibilities and opens the door to direct investigations of their contribution to reproductive isolation among naturally hybridizing species.</p></div

Two-locus genotypes of green and white seedlings at markers linked to <i>hl13</i> and <i>hl14</i>.

<p>Count represents the number of F2s with a given genotype. Genotypes are homozygous <i>M</i>. <i>guttatus</i> (‘G’), homozygous <i>M</i>. <i>nasutus</i> (‘N’), and heterozygous (‘H’). The vast majority (92%) of white F2s carry the G:N genotype, whereas green F2s carry all genotypes except G:N. Sample size is 2,652, which represents the subset of our mapping population that was genotyped with markers M208, M236, M241, and M132.</p

Misexpression of chloroplast genome in white seedlings.

<p>Heat map displaying expression patterns of 52 chloroplast genes from seven chloroplast gene families in seedlings from DPR102<i>-gutt</i>, DPR104<i>-nas</i>, Green F2s and White F2s. Z-scores of normalized FPKM values were calculated for each row to illustrate relative expression differences among genes. Bars on left of heatmap indicate whether genes are primarily transcribed by PEP, PEP and NEP, or NEP RNA polymerases. *denotes genes that are significantly differentially expressed between white seedlings and all green seedlings (DPR102<i>-gutt</i>, DPR104<i>-nas</i>, and Green F2s).</p

Hypothetical model for the evolution of <i>pTAC14</i>.

<p>Prior to gene duplication the ancestral <i>M</i>. <i>guttatus-</i>like population harbored genetic variation for <i>pTAC14</i> at <i>hl13</i> (different colored boxes represent genetic variation at <i>pTAC14</i>). During speciation, <i>M</i>. <i>nasutus</i> acquired a copy of <i>pTAC14</i> harboring ‘blue’ variation (left). Similarly, the <i>M</i>. <i>guttatus-</i>specific duplication involved a closely related <i>‘</i>blue’ <i>pTAC14</i> variant. Contemporary variation within <i>M</i>. <i>nasutus</i> and <i>pTAC14</i> variants located at <i>hl14</i> resemble one another genetically due to common ancestry, while <i>pTAC14</i> variants at <i>hl13</i> in <i>M</i>. <i>guttatus</i> likely continue to harbor considerable genetic variation, including variants that contain functional (IM62) and non-functional (DPR102<i>-gutt</i>) variants.</p

<i>pTAC14</i> gene structure and neighbor-joining tree.

<p>(A) Gene model of <i>pTAC14</i> in <i>Mimulus</i> is shown along the top. A frameshift mutation in the G1 copy of <i>pTAC14</i> (DPR102<i>-gutt</i>, <i>Mg</i>.<i>pTAC14_1</i>) is caused by the insertion of an adenine in the 7^th exon, highlighted with a box. (B) Unrooted neighbor-joining tree of <i>pTAC14</i> genes from DPR102<i>-gutt</i>, DPR104<i>-nas</i>, and the IM62 reference genome. Bootstrap support given at node and substitution rate shown for scale.</p

Duplicate copies of pTAC14 map to both hybrid lethality loci in <i>M</i>. <i>guttatus</i>.

<p>(A) Ten SNPs differentiate <i>Mg</i>.<i>pTAC14_1</i> (G1), <i>Mg</i>.<i>pTAC14_2</i> (G2), and <i>Mnas</i>.<i>pTAC14</i> (N1). (B) Phenotype: green (GRN) or white (WHT) F2. hl13 and hl14: genotype at flanking markers [G (DPR102<i>-gutt</i>), N (DPR104<i>-nas</i>, and G/N (heterozygous)]. N is sample size. Observed: Copies of <i>pTAC14</i> observed in each F2, consistent across all F2s for a given genotype. Note that individuals with DPR102<i>-gutt</i> alleles at hl13 always carry <i>Mg</i>.<i>pTAC14_1</i>, individuals with DPR102<i>-gutt</i> alleles at hl14 always carry <i>Mg</i>.<i>pTAC14_2</i>, and individuals with DPR104<i>-nas</i> alleles at hl13 always carry <i>Mnas</i>.<i>pTAC14</i>. (C) Location of different copies of pTAC14 based on our mapping experiment.</p

Population Genetics of the Rubber-Producing Russian Dandelion (Taraxacum kok-saghyz).

The Russian dandelion, Taraxacum kok-saghyz (TKS), is a perennial species native to Central Asia that produces high quality, natural rubber. Despite its potential to help maintain a stable worldwide rubber supply, little is known about genetic variation in this species. To facilitate future germplasm improvement efforts, we developed simple-sequence repeat (SSR) markers from available expressed-sequence tag (EST) data and used them to investigate patterns of population genetic diversity in this nascent crop species. We identified numerous SSRs (1,510 total) in 1,248 unigenes from a larger set of 6,960 unigenes (derived from 16,441 ESTs) and designed PCR primers targeting 767 of these loci. Screening of a subset of 192 of these primer pairs resulted in the identification of 48 pairs that appeared to produce single-locus polymorphisms. We then used the most reliable 17 of these primer pairs to genotype 176 individuals from 17 natural TKS populations. We observed an average of 4.8 alleles per locus with population-level expected heterozygosities ranging from 0.28 to 0.50. An average pairwise FST of 0.11 indicated moderate but statistically significant levels of genetic differentiation, though there was no clear geographic patterning to this differentiation. We also tested these 17 primer pairs in the widespread common dandelion, T. officinale, and a majority successfully produced apparently single-locus amplicons. This result demonstrates the potential utility of these markers for genetic analyses in other species in the genus

Principal coordinates analysis (PCoA) based on a genetic distance matrix of individuals within the 17 sampled populations.

<p>The first two coordinates explain 9.27% and 7.90% of the observed variation, respectively.</p

Map indicating the locations of the 17 sampled Russian dandelion populations.

<p>Blue dots represent the locations of the populations. The x- and y-axes represent longitude and latitude, respectively. The main and inset maps were made using the R libraries ‘maps’ and ‘maptools’, respectively [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0146417#pone.0146417.ref030" target="_blank">30</a>].</p