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A second hypothesis is that SDTF is more generally dispersal-limited, thus restricting the ability of lineages to radiate subsequent to their arrival into expanding habitat. Such a scenario might offer newly available niche space for lineages to occupy via dispersal from outside the regional source pool. Previous studies have found a significant degree of genetic differentiation among geographically isolated populations across dry forest habitats, supporting the idea that these dry-forests are dispersal-limited Pennington et al.
Furthermore, at least one of the two lineages Bunchosia [20 sp. Such lineages are likely to more easily migrate and radiate across a landscape via allopatric speciation. This is compounded by the fact that the formation of SDTF was not likely contiguous, both spatially and temporally Graham and Dilcher, New fragments of SDTF likely arose at different times and in different regions of Mexico, which might have greatly facilitated the continuous establishment of new Malpighiaceae lineages via dispersal from external source pools.
In combination, these processes might act to limit the overall diversification of single Mexican introductions, and help explain the pattern of frequent and continued dispersal of new lineages into this biome. The predominance of dispersal in the formation of a regional species pool has been shown elsewhere, including in the California chaparral Ackerly, , the Atacama Desert Heibl and Renner, , and in temperate, post-glacial habitats Williams et al.
However, these and related studies are commonly restricted to a narrow window of time or to a single, relatively young clade. In our case, the overwhelming pattern of dispersal we identify spans a wide period of time as well as a large, diverse plant clade. This raises the possibility that the characterization of species pools being dominated by single lineages that moved into a region and subsequently radiate, such as in the Andes Hughes and Eastwood, or on remote islands Baldwin and Sanderson, ; Emerson, , may be exceptions rather than the rule of species pool assembly.
A more general pattern, especially with regard to the phylogenetic diversity of a species pool, might instead be the steady recruitment of independent lineages via dispersal over tens of millions of years, most of which exhibit modest rates of in situ diversification. Our analyses of trait adaptation to precipitation provide direct insights for more clearly interpreting the spatial and temporal origins of xeric adaptations by Mexican Malpighiaceae.
An emerging question in the field of biogeography is when did traits relevant to community assembly originate Ackerly, ; Cavender-Bares et al. Specifically, did Mexican Malpighiaceae evolve adaptations to xeric habitats elsewhere ex situ , i. We found that the timing of adaptation to these two key climate traits contrast sharply in relation to when lineages become restricted to Mexico Figures 4 , S4, S5.
Thus, lineages that subsequently became geographically restricted to Mexico were likely pre-adapted for living in relatively drier environments. This climatic adaptation appears to have arisen largely in South America Figure S4. In contrast, adaptation to extreme precipitation seasonality evolved largely concurrent with or after Malpighiaceae became restricted to Mexico Figures 4 , S5. We interpret these results to indicate that adaptations to precipitation seasonality largely arose in situ in Mexico as the abiotic conditions of SDTF were developing in this region Figure S5.
This pattern is supported by recent findings that identified a lag time in the adaptation of lineages to dry environments following their arrival into the Atacama Desert in South America Guerrero et al. Our results, however, provide a more nuanced perspective of in situ adaptation to dry forest environments and illuminate the timing of the origin and expansion of modern SDTF in Mexico. This suggests that although SDTF appears to have arisen in Mexico during the late Oligocene, it was likely geographically restricted at the time. It did not expand greatly until the mid-Miocene.
Furthermore, this pattern more broadly coincides with global aridification that began during the Miocene, which marked the worldwide expansion of grasslands and succulent biomes Cerling et al. Our results for Malpighiaceae further indicate that the expansion and widespread establishment of SDTF in the mid-Miocene marks a transition in the temporal pattern of adaptation to precipitation seasonality. These younger lineages appear to have arisen from ancestors that adapted to precipitation seasonality in Mexico and Central America, but subsequently became geographically restricted to Mexico.
These patterns collectively illuminate the timing of the origin and expansion of modern SDTF in Mexico, and indicate that this biome more recently served as an important species pool for other SDTFs across the Neotropics. It is important to keep in mind that the formation of the SDTF biome in Mexico occurred over millions of years, which appears to have afforded the earlier inhabitants of this region the time necessary to adapt to the novel abiotic conditions that define this biome today.
If our hypothesis is correct, we should observe a pattern of more gradual adaptation to precipitation seasonality for dry periods that are consistent with intermediate historic levels i. When we perform this exercise, we observe a clear pattern of earlier adaption to these historic levels as expected under our hypothesis Figures 4 , S5. The extent to which this in situ adaptation occurred within the geographic footprint of the biome itself, vs. However, we would expect in situ adaptation within the biome for many of these lineages.
Further investigations using additional taxon sampling and far better geographic reconstructions of this biome throughout the Cenozoic would be required to determine this more confidently. Additionally, studies of recent range expansions and adaptions to novel environments could shed insight into this scenario. Nevertheless, the lag times we identify raise concerns about using modern biome categorizations as static characters for phylogenetic character state reconstruction Davis et al.
In particular, our study indicates that ancestral reconstructions of biomes as static characters are problematic if the abiotic parameters that define these biomes today are much more recently evolved than the clades that inhabit them. Instead, our results suggest that inferring the evolution of key parameters that characterize these biomes e.
Editors: Fittkau, E.J., Illies, J., Klinge, H., Schwabe, G.H. With 'Biogeography and Ecology in South America' as the general theme, a total of twenty-nine contributions by thirty authors is offered here in two volumes, being volumes 18 and 19 of the Monographiae Biologicae. Biogeography and Ecology in South-America. Volume II. Editors: Fittkau, E.J., Illies, J., Klinge, H., Schwabe, G.H., Sioli, H. (Eds.).
The assembly of a biome's flora depends on the complex interplay of dispersal, adaptation, and in situ diversification Emerson and Gillespie, These processes in turn depend on both the geographic proximity and ecological similarity between the source pool and the biome in question Emerson and Gillespie, ; Edwards and Donoghue, Our results additionally demonstrate that these processes are not static and change over evolutionary time. This has important implications for the composition of SDTF in Mexico to the formation of regional species pools and biomes more broadly.
In the case of the formation of the Mexican Malpighiaceae flora, we found that changes in the geographic connectivity between South America and Mexico in the Miocene lead to dramatic changes in dispersal patterns from South America. Initially, lineages were limited to less frequent, longer-distance dispersal from South America. But increasingly the availability of Central America permitted more frequent, shorter-distance dispersal, facilitating vastly greater migration to Mexico starting in the mid-Miocene.
The increased rate of dispersal, in turn, significantly influenced the composition of Mexican Malpighiaceae.
While much of the extant species diversity in Mexico derives from in situ diversification, the overwhelming majority of phylogenetic diversity derives from multiple, independent introductions from South American ancestors spanning the phylogenetic breadth of the Malpighiaceae clade. Furthermore, climatic conditions that define the extant SDTF biome appear to have changed through time.
While most lineages arrived in Mexico pre-adapted to one key factor of SDTF, total annual precipitation, these lineages subsequently adapted to another major axis, seasonal dry periods in situ.
In this case, in situ adaption appears to have occurred gradually, over many millions of years, coincident with mountain building that established the geological conditions that maintain the biome today. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We thank C. Anderson, W.
Anderson, J. Beaulieu, S. Cappellari, M. Gomez, D.
Rabovsky, C. Webb, W.
Zhang, and members of the Davis laboratory for technical assistance and valuable discussions. This paper is dedicated to William R. Anderson—friend, and lifelong student of Malpighiaceae. Ackerly, D. Adaptation, niche conservatism, and convergence: comparative studies of leaf evolution in the California chaparral. The origin of the Malpighiaceae—The evidence from morphology.
Origins of Mexican Malpighiaceae. Antonelli, A. Tracing the impact of the Andean uplift on Neotropical plant evolution. Arakaki, M. Contemporaneous and recent radiations of the world's major succulent plant lineages. Baldwin, B. Age and rate of diversification of the Hawaiian silversword alliance Compositae.
Becerra, J. Timing the origin and expansion of the Mexican tropical dry forest. Bell, C. Phylogeny and biogeography of Valerianaceae Dipsacales with special reference to the South American valerians. Berggren, W.
Berggren, D. V Kent, M. Aubry, and J. Cameron, K. Molecular systematics of Malpighiaceae: evidence from plastid rbcL and matK sequences. Cavender-Bares, J. The merging of community ecology and phylogenetic biology. Cerling, T. Nature , — Expansion of C4 ecosystems as an indicator of global ecological change in the late Miocene. Christopoulos, D. Clayton, J. Recent long-distance dispersal overshadows ancient biogeographical patterns in a pantropical angiosperm family Simaroubaceae, Sapindales. Cody, S.
The Great American Biotic Interchange revisited.