Molecular Natural History is a series of posts highlighting what genetic data has revealed about some of my favorite organisms. There’s no rhyme or reason to what species I’ll feature for this, beyond the fact that they’ve made me stop and look closer when I see them along a trail or in my neighborhood. If you’d like to write about the molecular natural history of a favorite taxon, why not pitch a guest post?
Choosing a favorite wildflower is a challenge for anyone with a little depth of botanical experience, but if I had to pick one I appreciate purely for its decorative presence on the landscape, it would probably be a lupine.
Genus Lupinus includes hundreds of species across the globe, with centers of diversity in the mountain ranges that run down the western spines of North and South America. In spring and summer, you don’t need to hike far into the Rockies or the Cascades or the Sierras before you’ll find their racemes of blue-and-white or yellow or pink flowers marking the edge of the trail. In much of Western North America, you can see multiple species in a few miles of hiking.
Lupine flowers are the prototype of the “papilionaceous” — that is, butterfly-shaped — flower structure distinctive to the legume family. The shape is clearest in profile, resembling the folded wings of a butterfly. It is formed, in fact, from five petals: a “keel” is the fusion of two petals, like hands cupped together, or the bottom of a rowboat; then two “wings” on either side close around the keel; and a broad, reflexed “banner” extends above them all.
Inside, the stamens are partially fused around the pistil, and not especially accessible to a visiting pollinators. Some legumes with this floral structure are fully cleistogamous, the stamens depositing pollen onto their own pistils before the flower is even properly open. Lupines are self-compatible, but they’re generally insect-pollinated, and the proportion of self-fertilization depends on circumstances and life history. Some species in the genus are annuals, such as the tiny Lupinus bicolor at the top of this post, and they may self-pollinate to improve the odds that their single growing season yields seeds. Not all annual lupines do this, however, and perennial species, which have multiple years of reproductive opportunities, may be more likely to wait for “outcross” pollen from another plant. A genetic study of perennial bush lupine, Lupinus arboreus, for instance, found that diversity at five allozyme loci was consistent with outcrossing in about 78% of matings.
The papilionaceous flower structure controls how potential pollinators access the flower and reduces the number of pollinator species that may visit it. This specificity of pollinator interaction probably make plant lineages with bilaterally symmetric flowers, like lupines, more prone to evolving new species — it’s easier for populations to end up using different pollinators, which frees them to evolve differences in other features. Add in the capacity to self-pollinate — which means that a single seed in an isolated patch of habitat can give rise to a whole population — and you have a recipe for rapid diversification. Across the rugged terrain of western North and South America, lupines have done exactly that.
A 2012 study of the New World lupines reconstructed relationships, and timing of speciation events, from sequences of five nuclear and six chloroplast loci in 122 species. Given the timing of speciation events, the authors could identify significant changes in the rate of species formation across the phylogeny, and pinpointed three periods in which lupine species accumulated with unusual speed: 6.5 million years ago, when one lineage diversified in the grasslands of eastern South America; 4.6 million years ago, in the mountain west of North America; and 2.7 million years ago, as sister clades formed in the highlands of central Mexico and the Andes.
Tracing the ecologies and life histories of the sampled species back to their likely ancestral conditions, the authors found that all three of these radiations were associated with shifts from annual towards perennial life histories, and the two more recent ones matched transitions from lowland into mountainous habitats. The authors suggest that this is consistent with species formation driven by ecological opportunity — perennial life history making new habitats accessible for diverse new lupine species — and “montane mosaics”, patches of habitat created by rugged terrain, with lots of opportunities for spatial isolation to let populations evolve differences. The former may have a role for adaptation, but the latter would suggest nonadaptive radiation.
A more recent study more clearly pinpoints a role for adaptation in the flowering of lupine diversity. Its authors tested for evidence of natural selection acting on thousands of genes, using a common approach of comparing how rapidly each gene acquired nonsynonymous mutations to the rate of synonymous mutations. Synonymous mutations to DNA sequence don’t change the protein produced by that sequence, so they’re expected to evolve without the influence of natural selection; nonsynonymous mutations do change proteins, so they may be selected for — or against. The North American perennial and Andean lupine clades had substantially more genes where nonsynonymous mutations exceeded synonymous ones — consistent with natural selection changing those genes — compared to the North American annual lupines, or to other diverse plant genera like sunflowers, nightshades, and rice.
So the diversity of New World lupines looks to be the product of not one, but two or maybe three adaptive radiations, rapid accumulations of new species as populations evolved in response to natural selection in complex, mountainous geography. Selection probably didn’t act alone, though. Geographic isolation, and isolation created by specialized pollinator associations, means natural selection can more easily push isolated populations toward speciation.
And that — natural selection abetted by some geographic and geological luck — is why you can see lupines in multiple colors, and even multiple growth forms, on a single hike through the hills of Big Sur.
References
Drummond CS, RJ Eastwood, STS Miotto, and CE Hughes. 20112. Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): Testing for key innovation with incomplete taxon sampling. Systematic Biology. 61(3): 443–460. doi.org/10.1093/sysbio/syr126
Kittelson PM and JL Maron. 2000. Outcrossing rate and inbreeding depression in the perennial yellow bush lupine, Lupinus arboreus (Fabaceae). American Journal of Botany. 87(5): 655-660. doi.org/10.2307/2656851
Nevado B, GW Atchison, CE Hughes, and DA Filatov. 2016. Widespread adaptive evolution during repeated evolutionary radiations in New World lupins. Nature Communications. 7, 12384 doi.org/10.1038/ncomms12384
Sargent RD. 2004. Floral symmetry affects speciation rates in angiosperms. Proc. Royal Soc. B 271, 603-608. doi.org/10.1098/rspb.2003.2644
Yoder JB, E Clancey, S Des Roches, JM Eastman, L Gentry, WKW Godsoe, T Hagey, D Jochimsen, BP Oswald, J Robertson, BAJ Sarver, JJ Schenk, S Spear, and LJ Harmon. 2010. Ecological opportunity and the origin of adaptive radiations. J. Evolutionary Biol. 23(8): 1581-96. doi.org/10.1111/j.1420-9101.2010.02029.x
Yoder JB, G Gomez, and CJ Carlson. 2020. Zygomorphic flowers have fewer potential pollinators. Biology Letters. 16(9): 20200307. doi.org/10.1098/rsbl.2020.0307
