Pleistocene aridification underlies the evolutionary history of the Caribbean endemic, insular, giantConsolea(Opuntioideae)

Abstract

Premise The Caribbean islands are in the top five biodiversity hotspots on the planet; however, the biogeographic history of the seasonally dry tropical forest (SDTF) there is poorly studied. Consolea consists of nine species of dioecious, hummingbird‐pollinated tree cacti endemic to the West Indies, which form a conspicuous element of the SDTF. Several species are threatened by anthropogenic disturbance, disease, sea‐level rise, and invasive species and are of conservation concern. However, no comprehensive phylogeny yet exists for the clade. Methods We reconstructed the phylogeny of Consolea, sampling all species using plastomic data to determine relationships, understand the evolution of key morphological characters, and test their biogeographic history. We estimated divergence times to determine the role climate change may have played in shaping the current diversity of the clade. Results Consolea appears to have evolved very recently during the latter part of the Pleistocene on Cuba/Hispaniola likely from a South American ancestor and, from there, moved into the Bahamas, Jamaica, Puerto Rico, Florida, and the Lesser Antilles. The tree growth form is a synapomorphy of Consolea and likely aided in the establishment and diversification of the clade. Conclusions Pleistocene aridification associated with glaciation likely played a role in shaping the current diversity of Consolea, and insular gigantism may have been a key innovation leading to the success of these species to invade the often‐dense SDTF. This in‐situ Caribbean radiation provides a window into the generation of species diversity and the complexity of the SDTF community within the Antilles.

Phylogenomics of the Caribbean melocacti: Cryptic species and multiple invasions

“…Phylogenetic work on Caribbean cacti has been further clarifying our understanding of the origin and evolution of the group in the Antilles, including positing Pleistocene drying events as a major driver of diversification across the islands (e.g., Majure & al., 2012, 2014; Franck & al., 2013; Barrios & al., 2020). Recent studies using chloroplast genomes across a number of different groups of Cactaceae emphasized the utility of those data for resolving deep phylogenetic as well as species‐level relationships in both of the major clades of the family, Cactoideae and Opuntioideae (Majure & al., 2019, 2021a,b; Köhler & al., 2020; Breslin & al., 2021). However, the resolving power of these data has not yet been tested in the species‐rich genus Melocactus , which is known for its diversity in the Antilles.…”

Evolutionary Genetics of Cacti: Research Biases, Advances and Prospects

“…For example, different methods to sequence a reduced representation of genomes have been used in evolutionary studies on cacti, resolving rapid and recent diversification in this group (e.g., [ 50 , 62 , 63 ]). In addition, de novo assembled genomes, transcriptomes, and plastomes have been successfully used in some cacti groups (e.g., [ 32 ]). These recently available genomics data are a valuable source to assist target enrichment sequencing approaches, enabling the identification of hundreds of orthologous regions (e.g., [ 64 ]).…”

“…Geomorphologic events, such as the uplift of the Andes, Trans Mexican Volcanic Belt structures, and geomorphological compartmentalization of the Brazilian Central Plateau, also influenced the distribution and expansion of cactus species [ 16 , 21 , 81 , 82 , 83 ]. The “Neogene aridification” theory advocates the expansion and recent radiation of the Cactaceae in the last 35 Ma (Miocene to Pliocene) [ 1 , 2 , 13 , 32 , 84 ]. The “Riverine” theory was recovered only once, associated with the genus Pilosocereus and the eastern Brazilian rivers, such as the Sao Francisco and Doce rivers [ 85 ].…”

“…Moreover, as many species may hybridize in nature (e.g., [ 13 , 27 , 28 ]), cacti may provide many insights into hybrid zones, species cohesion, and species delimitation. Finally, due to its intrinsic association with drought stress, cacti are useful models for biogeographic approaches aiming to investigate the effects of Quaternary climate oscillations on xeric biomes (e.g., [ 21 , 29 , 30 , 31 , 32 ]). As a result, many studies with an evolutionary focus have been conducted on cacti in recent decades.…”

A New Approach Using Targeted Sequence Capture for Phylogenomic Studies across Cactaceae

“…However, most phylogenetic reconstructions have been based solely or mostly on plastid data derived from Sanger sequencing methods and oftentimes using just a handful of loci (e.g., [ 3 , 4 , 5 , 6 , 7 , 8 , 9 ]). Arakaki et al [ 10 ] employed a combination of plastome and Sanger sequencing data to test the diversification of the family, and more recently transcriptome data (Walker et al 2018), as well as plastome datasets [ 11 , 12 , 13 , 14 , 15 ] have been utilized to more fully resolve species limits and deep phylogenetic history in the family. However, nuclear probe sets derived from single-copy loci, which are commonly used in other groups of Angiosperms [ 16 ], as well as other vascular and non-vascular plants [ 17 ], have not yet been generated for the family.…”