The evolutionary origins of morphological diversity in Cactaceae

Dr Jamie Thompson

School of Biological Sciences, The University of Reading, United Kingdom (, X: Jamie_T42)

Cactaceae are among the most celebrated angiosperm families, due to their species richness, dramatic adaptations to water scarcity, and charismatic morphological variation. The ~1,850 species have evolved a vast variety of morphological forms including tiny buttons, massive “trees”, drooping epiphytes, and impressive barrels. This remarkable variation has allowed cacti to adapt to, and thrive in, diverse New World biomes including arid deserts, humid rainforests, and high-altitude Andean plateaus. We have a good understanding of how morphological evolution shaped cactus diversity, with recent studies demonstrating the dependence of speciation and extinction rate on different morphologies. However, we know remarkably little about the evolutionary origins of morphological diversity in the first place. Broadly speaking, cacti vary morphologically at least >2,500-fold, considering the smallest cacti (Blossfeldia liliputana) and the tallest (in Carnegiea and Pachycereus). This variation is far greater than is found in other well-studied groups, such as mammals, in which body size varies ~570-fold. Furthermore, morphological variation in cacti has evolved in a much shorter amount of evolutionary time than mammals (~37-27 million years (Ma) compared to ~186-168 Ma). This represents a remarkable but unexplored area of evolutionary history.

Using phylogenetic comparative methods to reveal origins of evolutionary diversity

Investigations into morphological evolution rely on phylogenetic comparative methods (PCMs), a powerful suite of statistical tools that reconstruct evolutionary history. PCMs were traditionally used to simply correct for the statistical non-independence of species, which are similar due to shared ancestry. However, new methods make use of the tree topology to explain rates of morphological evolution. PCMs can reveal the tempo of evolution, distinguishing between the “early burst” model found in Darwin’s finches, and more-recent evolution occurring nearer the tips. PCMs can also reveal whether evolution is punctuated or gradual, a major hypothesis in evolution going back to Charles Darwin. Crucially, PCMs can identify lineages in which the rate of morphological evolution has dramatically accelerated or decelerated. These departures from background rate can indicate natural selection, possibly from a driver, which could be biotic (e.g. pollinators, adaptations) or abiotic (e.g. precipitation, aridity). Although never performed in a plant lineage, similar PCM research in animals has revealed extraordinary evolutionary patterns. These include relationships between eye size evolution and nocturnality; testes mass evolution and monogamy; biting force evolution and ecological strategy; and body mass evolution and temperature.

Plant height, a “key but neglected” trait in evolutionary research

We have investigated the evolution of cactus size, which we have measured as height (or length for sprawling species, such as epiphytes). Size is a critical component of eco-evolutionary strategies, and is strongly influenced by biophysical constraints, geographic distributions, ancestry, and climate. Knock-on effects of size evolution are numerous, including shaping diversification rates, generation times, and species richness patterns. Although size is just one morphological metric, it captures a large proportion of overall variation. This is because many biological phenomena correlate with size across the Tree of Life including metabolism, lifespan, and reproductive strategy. For these reasons, many PCM analyses into origins of morphological diversity focus on size. Zoological researchers typically analyse body mass instead of height, since it captures variation associated with different body plans. However, this is not possible for cacti because plant mass is rarely, if ever, measured. Nevertheless, height has strong explanatory power in the evolution of another succulent lineage, the Alooideae (https://doi.org/10.1371/journal.pone.0233597). Paraphrasing the authors of this study, height is a “key determinant” of plant evolution but remains “neglected” in research.

Making use of the most comprehensive phylogenetic tree and eco-evolutionary dataset for cacti I recently reconstructed the largest molecular phylogeny of cacti comprising >1,000 species and assembled a dataset of 39 abiotic and biotic variables. This has been published in Nature Communications as part of a paper using machine learning to disentangle the complexity underlying cactus diversification (https://doi.org/10.1038/s41467-024-51666-2). With the BCSS fund, I have employed an incoming PhD student at the University of Reading over summer (Catherine Martinez) to work on this data. We have updated the database for the many more height records that have been published since initial submission of the Nature Communications article, and we have reclassified growth forms into a more nuanced system. This has been in collaboration with Michiel Pillet (University of Arizona), and Dr Alastair Culham and Andrew Gdaniec (University of Reading). Working with Professor Chris Venditti and Dr Andrew Meade (University of Reading), we have used PCMs to reveal variable rates of morphological evolution and have uncovered very exciting patterns. We are currently finalising our results and preparing a manuscript for publication. I am very grateful for this BCSS Research Grant, without which, this work would not have been possible. The grant has supported early career researchers both pre-and-post PhD. It also enabled the creation of international collaborations spanning diverse disciplines within evolutionary biology and conservation. Our research will contribute to our understanding of morphological variation in Cactaceae, one of the most charismatically diverse, yet most threatened, plant families.

Figure 1: The time-calibrated molecular phylogeny of Cactaceae (left panel), with major branches indicated (A = Cactoideae, B = Opuntioideae, C = the Mammilloid clade). The phylogenetic distribution of cactus height, and coarsely classified growth forms (right panel), replotted using preliminary data from https://doi.org/10.1038/s41467-024-51666-2.

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