STUDENT DIGEST

Different modes of trait evolution weave a rich tapestry of functional diversity in the Neotropics

Yago Barros-Souza, PhD candidate
Universidade de São Paulo, Ribeirão Preto, Brazil Universidade Federal de São Carlos, São Carlos, Brazil

The astonishing functional diversity of neotropical ecosystems has been largely attributed to the dynamics of major geological and climatic events. The uplift of the Andes, Pleistocene climatic oscillations,decline in atmospheric CO₂, and Miocene marine flooding, all resulted in new ecosystems and biomes and also drove trait evolution. For example, the increasing dominance of flammable grasses, attributed ultimately to drops in atmospheric CO₂ levels (Jaramillo, 2023): triggered the assembly of the young South American savannas, resulting in in situ adaptations to fire in numerous independent plant lineages (Simon et al., 2009). On the other hand, pre-existing traits may also have enabled lineages to colonise new environments, provided those traits conferred fitness advantages in those environments (i.e., pre-adaptation, or ‘exaptation’ sensu Gould & Vrba, 1982). Aerial roots in mangrove species, for example, probably arose as the result of selection for oxygen transport and nutrient uptake in non-mangrove saline habitats, and were only later co-opted as support structures in mangroves (Sahu et al., 2016). Therefore, both adaptation and pre-adaptation can lead to optimal ecological performance through trait-environment matching.

In a recent paper published in Global Ecology and Biogeography, Velásquez-Puentes et al. (2023) addressed whether trait and environmental niche evolution are correlated and what is the primary mode of trait evolution relative to environment. To answer these questions, they focused on the genus Swartzia Schreb. (Leguminosae, Papilionoideae): an emblematic neotropical legume radiation. Swartzia provides a suitable model to investigate trait-environment patterns and their underlying causes due to its high species and morphological diversity and relatively wide geographic distribution predominantly in rain forests, but also in other biomes, such as savannas and dry forests (Torke and Schaal, 2008). Velásquez-Puentes et al. hypothesised that (H1) trait-environment matching is evident in Swartzia; (H2) trait and environmental niche evolution are correlated; and (H3) pre-adaptation is the predominant mode underlying trait-environment matching. The authors reconstructed a phylogeny sampling 89 Swartzia taxa (ca. 40% of the total) and assembled trait and environmental data encompassing leaflet, fruit, and petal trait dimensions and water deficit, soil texture, soil fertility, and temperature environmental factors. Using phylogenetic comparative methods, Velásquez-Puentes et al. found a positive correlation between leaflet area and annual precipitation/temperature, and a negative correlation between petal width and annual temperature, supporting H1. They also found strong support for correlated evolution between leaflet size, presence or absence of petals, and climate niche evolution, suggesting that transitions between trait states are contingent on transitions between environmental states (H2). Finally, leaflet size shifts preceded environmental shifts (pre-adaptation) while shifts between presence and absence of petals follow environmental shifts (adaptation): suggesting that both adaptation and pre-adaptation shaped morphological diversity in Swartzia (H3). Neither fruit dimensions nor soil data showed a significant match with any other factor. Nonetheless, their results show that trait-environment matching shapes trait diversity in Swartzia and that trait evolution followed complex macroevolutionary trajectories in which Swartzia lineages evolved morphologically either by tracking abiotic conditions to which they were adapted or by adapting following transitions to new environments.

Swartzia species featuring some of the key traits addressed by Velásquez-Puentes et al. (A) Swartzia arborescens, apetalous flowers; (B) Swartzia grandifolia, petalous flowers; (C) Swartzia prolata, small leaflets; (D) Swartzia simplex, large leaflets. Photos: Benjamin Torke.

But what are the ecological associations that shaped these trait-environment correlations and what evolutionary mechanisms drove these distinct modes of trait evolution in Swartzia? Because the evolution of large and small leaflets facilitated transitions to wetter/warmer and drier/colder environments, the authors suggested that water and temperature stress impose limitations on leaflet size. Their results support a pre-adaptive mode of leaflet size evolution, suggesting that the current functional significance of different leaflet sizes may be distinct from the function they were originally selected for. Velásquez-Puentes et al. suggested that small leaflets, which can be an adaptation to drought (Bacelar et al., 2004): probably evolved first within rainforests, thereby facilitating subsequent colonisation of drier areas. Although the initial pressure for smaller leaflets in wet habitats is unknown, the authors suggested that local climatic gradients, genetic constraints, and/or herbivory may have influenced variation in leaflet size in rainforests. In contrast with leaf evolution, Velásquez-Puentes et al. found evidence for an adaptive mode of evolutionary loss of petals contingent on temperature, as Swartzia lineages lost petals only after colonisation of warmer habitats. This suggests that petal loss may be under positive selection due to heat stress and herbivory, as large petals may not be as efficient as small petals for heat regulation via transpiration (Descamps et al., 2020) and higher temperatures may increase herbivory (Hamman et al., 2021). Additionally, petal loss is common when pollinator-mediated selective pressures are absent due to evolution of other means to attract pollinators (Zhang et al., 2013). Indeed, pollination attraction in Swartzia is strongly mediated by visual cues (dimorphic stamens) and chemical signals (Basso-Alves et al., 2022).

Velásquez-Puentes et al. provide robust evidence that both adaptation and pre-adaptation shaped trait diversity and lineage composition of Swartzia across the Neotropics. Historical biogeographic origins of Swartzia in Amazonian rainforests and later dispersals and adaptations to adjacent habitats, is common in many plant and animal groups (Antonelli et al., 2018). Velásquez-Puentes et al. pave the way for future research to investigate whether different modes of trait evolution occur in a concerted way to shape the astonishingly high functional diversity of the Neotropics as a whole.

References

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