Lichter-Marck, I. H. | Search bioRxiv

bioRxiv2024

Phylogenomics of the North American Desert Radiation Linanthus (Polemoniaceae) Reveals Mixed Trait Lability and No Single Geographic Mode of Speciation

PremiseUnderstanding how arid-adapted plants have diversified in harsh environments is a central question in evolutionary biology. Linanthus (Polemoniaceae) occurs in biodiverse dry areas of Western North America and exhibits extensive floral trait variation, multiple color polymorphisms, differences in blooming time, and variation in life history strategies. Here, we reconstruct the evolutionary history of this group. MethodsWe generated restriction-site associated (ddRAD) sequences for 180 individuals and target capture (TC) sequences for 63 individuals, with complete species sampling. Using maximum likelihood and pseudo-coalescent approaches, we inferred phylogenies of Linanthus and used these phylogenies to model the evolution of phenotypic traits and investigate the geographic speciation history of this genus. Key resultsShallow relationships are consistent and well supported with both ddRAD and TC data. Most species are monophyletic despite rampant local sympatry and range overlap, suggesting strong isolating barriers. The non-monophyly of some species is possibly due to rapid speciation or issues with current species delimitation. Perenniality likely evolved from annuality, a rare shift in angiosperms. Night blooming evolved three times independently. Flower color polymorphism is an evolutionarily labile trait and is likely ancestral. No single geographic mode of speciation characterizes the radiation but most species overlap in range, suggesting they evolved in parapatry. ConclusionsOur results illustrate the complexity of phylogenetic inference for recent radiations, even with multiple sources of genomic data and extensive sampling. This analysis provides a foundation to understand aridity adaptations, such as evolution of flower color polymorphisms, night blooming, and perenniality, as well as speciation mechanisms.

evolutionary biology↗

bioRxiv2022

Edaphic specialization onto bare, rocky outcrops as a factor in the evolution of desert angiosperms

Understanding the processes that enable organisms to shift into more arid environments as they emerge is critical for gauging resilience to climate change, yet these forces remain poorly known. In a comprehensive clade-based study, we investigate recent shifts into North American deserts in the rock daisies (Perityleae), a diverse tribe of desert sunflowers (Compositae). We sample Perityleae across two separate contact zones between tropical deciduous forest and desert biomes in western North America and infer a time-calibrated phylogeny based on target capture sequence data. We reconstruct biome shifts using Bayesian inference with paleobiome-informed models and find evidence for seven independent shifts into desert habitats since the onset of aridification in the late Miocene epoch. The earliest shift occurred out of tropical deciduous forests and led to an extensive radiation throughout North American deserts that accounts for the majority of extant desert Perityleae. Reconstructions of life history and micro-habitat in Perityleae reveal a correlation between a suffrutescent perennial life history and edaphic endemism onto rocky outcrops, an ecological specialization that evolved prior to establishment and diversification in deserts. That the insular radiation of desert rock daisies stemmed from ancestors pre-adapted for dry conditions as edaphic endemics in otherwise densely vegetated tropical deciduous forests in northwest Mexico underscores the crucial role of exaptation and dispersal for shifts into arid environments. Significance StatementThe environmentally stressful conditions found in desert regions have often been implicated as the main factor in the evolution of drought tolerance in desert plants. Yet many iconic desert plant lineages evolved prior to the recent emergence of widespread arid climates, suggesting an important role for pre-adaptation (exaptation). In the desert rock daisies (Perityleae), we provide empirical support for this view by showing that life history evolution associated with their ecological specialization onto rock outcrops was a precursor to their establishment and extensive diversification in North American deserts. We caution against assuming the presence of ancient dry biomes based on time-calibrated phylogenies and we emphasize the fundamental roles that exaptation and dispersal play during community assembly in novel environments.

evolutionary biology↗