Evolution of the monkeyflowers

Spring has finally come to us here in the North, and it's time to start thinking about planting. So, when I went to a seminar yesterday by John Willis, it was with dual motives.

Naturally, I was interested in hearing about his work relating the evolutionary ecology of Mimulus species to their genomics. As Willis and his many former and current lab members made clear in a recent review article in Heredity, monkeyflowers have become a really interesting model system for studying the dynamics of natural selection on genomes -- particularly, with relation to local ecological adaptation, and also with relation to speciation.

But I was also thinking about whether I could find a nice flower variety for my garden. I'm not particularly excited about peas, and I tolerate Arabidopsis when it comes up, but let's face it, it's not exactly a show flower. I'd love to get one of the prettier hawkweeds going (these have eponymical appeal as well as botanical interest) but the common ones are pretty boring.

Well, Willis's lab has been a center of development for Mimulus genetics. They have developed a store of SNPs and other markers (available at the Mimulus evolution website) for QTL mapping, and are using them to find genes responsible for ecological adaptations in different wild Mimulus populations. In the talk, Willis featured some of his collaborators' work finding genes involved in wet versus dry habitat adaptations and in early versus late flowering. These traits are connected to each other, as well as to other life history, plant size and flower size.

I left having my prior belief abundantly confirmed: botany is awesome. I mean, think about it. You can go outside, in your own neighborhood, and study biology. You can uproot your subjects and transplant them somewhere else, to watch how well they do. If they die, well, that's a data point, not an ethical emergency! Worried about gene-environment interactions? No problem, just put samples of all your subjects in the same greenhouse and wait. Need to isolate a QTL against a uniform genetic background? Cool, just repeatedly backcross it into an inbred line for a few generations, selecting for the trait each time. Want to study genetic correlations? Well, you can breed a thousand plants and select for any trait you want!

Oh, and if you want to, you can clone them.

Let's look at an example, from the Heredity review:

Recent work on floral evolution demonstrates that fundamental evolutionary questions can be addressed in Mimulus through the combination of field experiments and modern genomic approaches. Bradshaw et al. (1995, 1998) pioneered the application of genome mapping to study of ecologically important traits in Mimulus using RAPD and allozyme markers to map floral QTLs underlying the divergence between red-flowered, hummingbird-pollinated M. cardinalis and pink-flowered, bee-pollinated M. lewisii. The initial mapping experiments, with hybrid phenotypes measured in controlled greenhouse environments, revealed QTLs with major effects on virtually every floral character studied, from coloration and morphology to nectar production. To determine the effect of these QTLs on pollinator visitation and discrimination, Schemske and Bradshaw (1999) moved the genotyped hybrids to a field site near one of the few regions where the species coexist, and observed bee and hummingbird visitation behavior. Amazingly, the M. cardinalis allele at a single QTL, YELLOW UPPER (YUP), was responsible for an 80% loss of visitation by bee pollinators, and the M. cardinalis allele at a QTL responsible for variation in nectar production doubled hummingbird visitation (Schemske and Bradshaw, 1999). Bradshaw and Schemske (2003) subsequently created near-isogenic lines (NILs), where heterospecific alleles at YUP were reciprocally introgressed into the parental genetic backgrounds, and evaluated the response of pollinators to the NILs in the field. They observed an even clearer pattern of pollinator discrimination due to this locus, with a 74-fold increase in bee visitation in M. cardinalis NILs that carried the M. lewisii YUP allele, and a 68-fold increase in hummingbird visitation in M. lewisii NILs with the M. cardinalis YUP allele. Although the ecological context, in this case the community of potential pollinators, is certainly important to the evolution of new pollinator associations, these results also demonstrate that single genomic regions can have a large effect on major evolutionary transitions (Wu et al. 2008: 224-225).

The talk was mostly focused on the Mimulus guttatus complex, where some of the most pressing issues are life history, drought tolerance, and tolerance of high mineral concentrations, such as salt or copper. They were able to trace many QTL's of small effect with relation to the major differences in life history and moisture requirements in ecogeographic races of M. guttatus, to show that the within-population variation for these traits is caused by high-frequency (likely balanced) alleles rather than mutation-selection balance or rare alleles, and to find the correlated responses to selection of different plant traits based on different QTL's.

With respect to the genetics of speciation and ecogeographic race formation, they are helped by a long history of research on Mimulus. For example:

Macnair and Christie (1983) performed the first direct genetic analysis of hybrid incompatibilities in Mimulus. While studying the genetic basis of copper tolerance in California populations of M. guttatus, they noticed that some crosses between plants from the copper mines and certain other populations resulted in F1s that died as young seedlings. Further crossing studies revealed that the F1 lethality was caused by a deleterious epistatic interaction between the copper tolerance allele from the mine populations (or a gene tightly linked to it) and alleles at an unknown number of different loci from the other populations. Such deleterious interlocus interactions, usually referred to as DobzhanskyMuller (D-M) incompatibilities, are thought to be the major cause of low hybrid fitness in plants and animals (reviewed in Coyne and Orr, 2004). Remarkably, it appeared that natural selection for copper tolerance had indirectly resulted in the evolutionary origin of the hybrid incompatibility (Wu et al. 2008:226).

So yes, say what you want, botany is awesome. Plus, there's one more thing: I sat through an entire lecture about natural selection and ecological differentiation of species and races, and never once heard the word, "bottleneck." It was like traveling to some kind of bizarro world where biologists still read Darwin!

So we come down to the really difficult question: which variety am I going to plant? Mimulus glabratus is native here in Wisconsin, including Dane County, but it is not very showy, and prefers wet habitat. That makes it a poor fit for my native plant patch, which is dry/mesic, and which I never water unless the black-eyed Susans and bee balms start to wilt. Mimulus ringens is prettier, with bigger, lavender flowers, but also likes it wet.

I guess I'll have to keep looking. M. lewisii is a pretty variant, if I can find a good source for it, and I can keep it in one of the wetter corners of the yard. I would try for M. cardinalis, since we have hummingbirds sometimes, but I'd like to get Lobelia cardinalis going also, and it's a lot easier to find. Besides, it hardly looks like a monkey!

References:

Wu CA, Lowry DB, Cooley AM, Wright KM, Lee YW, Willis JH. 2008. Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100:220-230. doi:10.1038/sj.hdy.6801018