Neotropical niche evolution of Otoba trees in the context of global biogeography of the nutmeg family

Abstract

Aim Plant distributions are influenced by species’ ability to colonize new areas via long‐distance dispersal and propensity to adapt to new environments via niche evolution. We use otobas, a clade of ecologically dominant trees found in low‐to mid‐elevation wet forests, as a system to understand the relative importance of these processes within the Neotropics. Location Neotropics and global. Taxon Otoba and entire Myristicaceae. Methods We resolve the first phylogeny of Otoba the Angiosperms353 loci and plastome sequences from 13 accessions representing seven species. We pair this with the most densely sampled phylogeny of Myristicaceae to date, inferred using publicly available plastid data. We then use environmental niche modelling, biogeographical reconstruction, phylogenetic principle components analysis and Ornstein–Uhlenbeck models to infer biogeography and examine patterns of niche evolution. Results Myristicaceae has an Old World origin, with a single expansion into the Americas. Divergence dates, fossil evidence and a notable lack of long‐distance dispersal are consistent with a Boreotropical origin of Neotropical Myristicaceae. Mirroring the rarity of dispersal at the family level, Otoba's biogeography is marked by few biogeographical events: two expansions into Central America from a South American ancestor and a single dispersal event across the Andes. This limited movement contrasts with rapid climatic niche evolution, typically occurring across geographically proximate habitats. Main conclusion Contrasting with previous studies, long‐distance dispersal does not need to be invoked to explain the pantropical distribution of Myristicaceae, nor the biogeography of Otoba. This likely results from the family's relatively large seeds that are dispersed by large‐bodied vertebrates. Instead, rapid niche evolution in Otoba has facilitated its occurrence throughout mesic habitats of the northern Neotropics, including the Amazon rainforest and Andean montane forests. Otoba adds to a growing group of Neotropical plant clades in which climate adaptation following local migration is common, implying an important role of niche evolution in the assembly of the Neotropical flora.

Testing for changes in rate of evolution and position of the climatic niche of clades

“…Phylogenetic groups of species differ widely in their realised climatic niche. These differences may result from selective changes promoting niche widening or its converse (Aagesen et al 2016, Velasco et al 2018, Mondanaro et al 2020, Frost et al 2022), or be essentially neutral with regards to the fundamental niche (Bonetti & Wiens 2014, Boucher et al 2014, Saupe et al 2019). Whether or not the fundamental niche changes, identifying such differences has a huge impact on our understanding of species diversity patterns (Rolland & Salamin 2016, Olalla‐Tárraga et al 2017, Rolland et al 2018) of the link existing between climatic niche breadth and extinction risk (Wiens et al 2019, Taheri et al 2021) and of how climate change is impacting extinction and will continue to do so (Hanson et al 2020, Trisos et al 2020).…”

“…moves along the niche dimension), or both. Although there is solid recognition that phylogenetic effects must be considered to understand these changes under a proper comparative context (Kellermann et al 2012, Gutiérrez‐Pesquera et al 2016), most researchers just estimate the phylogenetic signal in bioclimatic variables, or rely on standard models of evolution such as BM (Münkemüller et al 2015, Corro et al 2021) or the Ornstein–Uhlenbeck process (Velasco et al 2018, Frost et al 2022). Yet, BM resides on assumptions that can be unrealistic for describing climatic niche evolution (Diniz‐Filho et al 2012, Kamilar & Cooper 2013), and even a significant signal does not indicate that the effect of shared ancestry on species' climatic niche is relevant (Freckleton & Jetz 2009, Cooper et al 2011, Münkemüller et al 2015).…”

Patterns in the genetic structure of 49 lowland rain forest tree species co‐distributed on opposite sides of the northern Andes

“…Widely distributed species often share broad similarities in genetic structure across their geographic ranges, reflecting similar demographic responses to climate change and landscape features (Avise, 2009; Hickerson et al., 2010). In lowland Neotropical rain forests, landscape features such as large rivers (Gascon et al., 2000; Naka & Brumfield, 2018; Nazareno et al., 2019), dry forest corridors (Costa, 2003), and mountain ranges (Bemmels et al., 2018; Frost et al., 2022; Serrano et al., 2021) frequently structure species distributions and spatial patterns of genetic variation. Mountain ranges have long been hypothesized to represent especially strong dispersal barriers to lowland rain forest species due to the high degree of specialization to narrow, stable climatic niches exhibited by tropical taxa (Janzen, 1967).…”

“…Mountain ranges have long been hypothesized to represent especially strong dispersal barriers to lowland rain forest species due to the high degree of specialization to narrow, stable climatic niches exhibited by tropical taxa (Janzen, 1967). At phylogenetic scales, the Northern Andean Cordilleras are an important biogeographic barrier to rain forest trees (Frost et al., 2022; Winterton et al., 2014), birds (Cracraft & Prum, 1988), and other vertebrates (Ron, 2000), yet many lowland rain forest tree species are distributed on both sides of the Andes (Bemmels et al., 2018; Dick et al., 2005; Gentry, 1982) in both the Amazon Basin and Central America (here broadly defined to also include the Chocó or the Pacific coastal region of Colombia and Ecuador; Figure 1). Little is known about how such species dispersed across the Andes and whether dispersal has left similar patterns of population genetic structure across multiple taxa.…”

“…, and mountain ranges Frost et al, 2022;Serrano et al, 2021) frequently structure species distributions and spatial patterns of genetic variation. Mountain ranges have long been hypothesized to represent especially strong dispersal barriers to lowland rain forest species due to the high degree of specialization to narrow, stable climatic niches exhibited by tropical taxa (Janzen, 1967).…”