David B. Lowry

The strength and genetic basis of reproductive isolating barriers in flowering plants

Speciation is characterized by the evolution of reproductive isolation between two groups of organisms. Understanding the process of speciation requires the quantification of barriers to reproductive isolation, dissection of the genetic mechanisms that contribute to those barriers and determination of the forces driving the evolution of those barriers. Through a comprehensive analysis involving 19 pairs of plant taxa, we assessed the strength and patterns of asymmetry of multiple prezygotic and postzygotic reproductive isolating barriers. We then reviewed contemporary knowledge of the genetic architecture of reproductive isolation and the relative role of chromosomal and genic factors in intrinsic postzygotic isolation. On average, we found that prezygotic isolation is approximately twice as strong as postzygotic isolation, and that postmating barriers are approximately three times more asymmetrical in their action than premating barriers. Barriers involve a variable number of loci, and chromosomal rearrangements may have a limited direct role in reproductive isolation in plants. Future research should aim to understand the relationship between particular genetic loci and the magnitude of their effect on reproductive isolation in nature, the geographical scale at which plant speciation occurs, and the role of different evolutionary forces in the speciation process.

A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation.

A set of experiments demonstrates the involvement of a chromosomal inversion in the adaptive transition between annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus

Mimulus is an emerging model system for the integration of ecological and genomic studies

The plant genus Mimulus is rapidly emerging as a model system for studies of evolutionary and ecological functional genomics. Mimulus contains a wide array of phenotypic, ecological and genomic diversity. Numerous studies have proven the experimental tractability of Mimulus in laboratory and field studies. Genomic resources currently under development are making Mimulus an excellent system for determining the genetic and genomic basis of adaptation and speciation. Here, we introduce some of the phenotypic and genetic diversity in the genus Mimulus and highlight how direct genetic studies with Mimulus can address a wide spectrum of ecological and evolutionary questions. In addition, we present the genomic resources currently available for Mimulus and discuss future directions for research. The integration of ecology and genetics with bioinformatics and genome technology offers great promise for exploring the mechanistic basis of adaptive evolution and the genetics of speciation.

ECOLOGICAL REPRODUCTIVE ISOLATION OF COAST AND INLAND RACES OF MIMULUS GUTTATUS

Abstract Adaptive divergence due to habitat differences is thought to play a major role in formation of new species. However it is rarely clear the extent to which individual reproductive isolating barriers related to habitat differentiation contribute to total isolation. Furthermore, it is often difficult to determine the specific environmental variables that drive the evolution of those ecological barriers, and the geographic scale at which habitat-mediated speciation occurs. Here, we address these questions through an analysis of the population structure and reproductive isolation between coastal perennial and inland annual forms of the yellow monkeyflower, Mimulus guttatus. We found substantial morphological and molecular genetic divergence among populations derived from coast and inland habitats. Reciprocal transplant experiments revealed nearly complete reproductive isolation between coast and inland populations mediated by selection against immigrants and flowering time differences, but not postzygotic isolation. Our results suggest that selection against immigrants is a function of adaptations to seasonal drought in inland habitat and to year round soil moisture and salt spray in coastal habitat. We conclude that the coast and inland populations collectively comprise distinct ecological races. Overall, this study suggests that adaptations to widespread habitats can lead to the formation of reproductively isolated species.

Finding the genomic basis of local adaptation: Pitfalls, practical solutions, and future directions

Uncovering the genetic and evolutionary basis of local adaptation is a major focus of evolutionary biology. The recent development of cost-effective methods for obtaining high-quality genome-scale data makes it possible to identify some of the loci responsible for adaptive differences among populations. Two basic approaches for identifying putatively locally adaptive loci have been developed and are broadly used: one that identifies loci with unusually high genetic differentiation among populations (differentiation outlier methods) and one that searches for correlations between local population allele frequencies and local environments (genetic-environment association methods). Here, we review the promises and challenges of these genome scan methods, including correcting for the confounding influence of a species’ demographic history, biases caused by missing aspects of the genome, matching scales of environmental data with population structure, and other statistical considerations. In each case, we make suggestions for best practices for maximizing the accuracy and efficiency of genome scans to detect the underlying genetic basis of local adaptation. With attention to their current limitations, genome scan methods can be an important tool in finding the genetic basis of adaptive evolutionary change.

Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus

Local adaptation is a well-established phenomenon whereby habitat-mediated natural selection drives the differentiation of populations. However, little is known about how specific traits and loci combine to cause local adaptation. Here, we conducted a set of experiments to determine which physiological mechanisms contribute to locally adaptive divergence in salt tolerance between coastal perennial and inland annual ecotypes of Mimulus guttatus. Quantitative trait locus (QTL) mapping was used to discover loci involved in salt spray tolerance and leaf sodium (Na(+)) concentration. To determine whether these QTLs confer fitness in the field, we examined their effects in reciprocal transplant experiments using recombinant inbred lines (RILs). Coastal plants had constitutively higher leaf Na(+) concentrations and greater levels of tissue tolerance, but no difference in osmotic stress tolerance. Three QTLs contributed to salt spray tolerance and two QTLs to leaf Na(+) concentration. All three salt-spray tolerance QTLs had a significant fitness effects at the coastal field site but no effects inland. Leaf Na(+) QTLs had no detectable fitness effects in the field. * Physiological results are consistent with adaptation of coastal populations to salt spray and soil salinity. Field results suggest that there may not be trade-offs across habitats for alleles involved in local salt spray adaptations.

Breaking RAD: an evaluation of the utility of restriction site-associated DNA sequencing for genome scans of adaptation

Understanding how and why populations evolve is of fundamental importance to molecular ecology. Restriction site‐associated DNA sequencing (RADseq), a popular reduced representation method, has ushered in a new era of genome‐scale research for assessing population structure, hybridization, demographic history, phylogeography and migration. RADseq has also been widely used to conduct genome scans to detect loci involved in adaptive divergence among natural populations. Here, we examine the capacity of those RADseq‐based genome scan studies to detect loci involved in local adaptation. To understand what proportion of the genome is missed by RADseq studies, we developed a simple model using different numbers of RAD‐tags, genome sizes and extents of linkage disequilibrium (length of haplotype blocks). Under the best‐case modelling scenario, we found that RADseq using six‐ or eight‐base pair cutting restriction enzymes would fail to sample many regions of the genome, especially for species with short linkage disequilibrium. We then surveyed recent studies that have used RADseq for genome scans and found that the median density of markers across these studies was 4.08 RAD‐tag markers per megabase (one marker per 245 kb). The length of linkage disequilibrium for many species is one to three orders of magnitude less than density of the typical recent RADseq study. Thus, we conclude that genome scans based on RADseq data alone, while useful for studies of neutral genetic variation and genetic population structure, will likely miss many loci under selection in studies of local adaptation.

Is local adaptation in Mimulus guttatus caused by trade‐offs at individual loci?

Local adaptation is considered to be the result of fitness trade‐offs for particular phenotypes across different habitats. However, it is unclear whether such phenotypic trade‐offs exist at the level of individual genetic loci. Local adaptation could arise from trade‐offs of alternative alleles at individual loci or by complementary sets of loci with different fitness effects of alleles in one habitat but selective neutrality in the alternative habitat. To evaluate the genome‐wide basis of local adaptation, we performed a field‐based quantitative trait locus (QTL) mapping experiment on recombinant inbred lines (RILs) created from coastal perennial and inland annual races of the yellow monkeyflower (Mimulus guttatus) grown reciprocally in native parental habitats. Overall, we detected 19 QTLs affecting one or more of 16 traits measured in two environments, most of small effect. We identified 15 additional QTL effects at two previously identified candidate QTLs [DIVERGENCE (DIV)]. Significant QTL by environment interactions were detected at the DIV loci, which was largely attributable to genotypic differences at a single field site. We found no detectable evidence for trade‐offs for any one component of fitness, although DIV2 showed a trade‐off involving different fitness traits between sites, suggesting that local adaptation is largely controlled by non‐overlapping loci. This is surprising for an outcrosser, implying that reduced gene flow prevents the evolution of individuals adapted to multiple environments. We also determined that native genotypes were not uniformly adaptive, possibly reflecting fixed mutational load in one of the populations.

Natural variation for drought-response traits in the Mimulus guttatus species complex

Soil moisture is a key factor affecting plant abundance and distribution, both across and within species. In response to water limitation, plants have evolved numerous morphological, physiological, and phenological adaptations. In both well-watered and water-limited conditions, we identified considerable natural variation in drought-related whole-plant and leaf-level traits among closely related members of the Mimulus guttatus species complex that occupy a diversity of habitats in the field. The self-fertilizing Mimulus nasutus and serpentine-endemic Mimulus nudatus demonstrated the overall greatest tolerance to soil water limitation, exhibiting the smallest reduction in seed set relative to well-watered conditions. This may be due in part to early flowering, faster fruit development, and low stomatal density. In contrast, flowering of coastal M. guttatus was so delayed that it precluded any seed production in water-limited conditions. This range of phenotypic responses to soil water deficit in Mimulus, coupled with developing genomic resources, holds considerable promise for identifying genomic variation responsible for adaptive responses to soil water availability.

Indirect Evolution of Hybrid Lethality due to Linkage with Selected Locus in Mimulus guttatus

Ecological selection on an adaptive allele causes a tightly linked hybrid incompatibility factor to rapidly hitchhike to high frequency in a population of the wildflower Mimulus guttatus.