Convergence, Consilience, and the Evolution of Temperate Deciduous Forests

Abstract

The deciduous habit of northern temperate trees and shrubs provides one of the most obvious examples of convergent evolution, but how did it evolve? Hypotheses based on the fossil record posit that deciduousness evolved first in response to drought or darkness and preadapted certain lineages as cold climates spread. An alternative is that evergreens first established in freezing environments and later evolved the deciduous habit. We monitored phenological patterns of 20 species of Viburnum spanning tropical, lucidophyllous (subtropical montane and warm temperate), and cool temperate Asian forests. In lucidophyllous forests, all viburnums were evergreen plants that exhibited coordinated leaf flushes with the onset of the rainy season but varied greatly in the timing of leaf senescence. In contrast, deciduous species exhibited tight coordination of both flushing and senescence, and we found a perfect correlation between the deciduous habit and prolonged annual freezing. In contrast to previous stepwise hypotheses, a consilience of independent lines of evidence supports a lockstep model in which deciduousness evolved in situ, in parallel, and concurrent with a gradual cooling climate. A pervasive selective force combined with the elevated evolutionary accessibility of a particular response may explain the massive convergence of adaptive strategies that characterizes the world's biomes.

Joint phylogenetic estimation of geographic movements and biome shifts during the global diversification ofViburnum

“…Specifically, our analyses are consistent with the view that the first viburnums had more-or-less entire (smooth) or irregularly toothed leaf margins, and that shifts into colder climates in multiple lineages were accompanied by the evolution of regularly toothed and/or lobed leaves (Schmerler et al, 2012;Edwards et al, 2016). Likewise, our findings support multiple shifts from the evergreen habit to the deciduous habit associated with adaptation to climates with prolonged winter freezing (Edwards et al, 2017). We note that there have also been reversals in both characters; for example, evergreen leaves with entire margins evolved in the cloud forests of the Neotropics.…”

“…Instead, it appears that there were multiple transitions from warm temperate into cold temperate forests. The earliest of these shifts, perhaps in the Late Eocene, occurred in two clades (Opulus and Pseudotinus) that today occupy the coldest climates of any Viburnum species (Edwards et al, 2017; forests. It appears that the Porphyrotinus clade occupied warm temperate forests when it entered North America, and it is possible that the occupation of this biome (with limited distribution in North America today) preceded both the shift into cold temperate forests to the north and cloud forests to the south.…”

“…Species were assigned affinities to one or more of four mesic forest biome classes, following Edwards et al (2017): tropical/subtropical (T), warm temperate (i.e., lucidophyllous) (W), cold temperate (Co), and/or cloud forest (Cl). Tropical forests experience limited seasonality (i.e., temperature and precipitation remain relatively stable and high throughout the year).…”

Macroevolutionary diversification rates show time-dependency

“…It was important that we gather data from as many different, independent sources as feasible rather than simply slicing up previously constructed "megaphylogenies" (66) for two reasons. First, very large trees are necessarily constructed using only the few genes that are widely available for many taxa; there is thus likely to be substantial uncertainty in both topology and divergence times (66)(67)(68) . Second, we wanted to minimize the correlation of error across datasets.…”

Modeling phylogenetic biome shifts on a planet with a past

“…Four of these fossils are older samples (48 to 33 Ma) from paleofloral 161 communities that we previously judged to be warm temperate or subtropical (Landis et al 162 2019). For our analyses in this study, we defined three mesic forest biomes based on 163 annual temperatures and rainfall patterns (Edwards et al 2017 forests, which include paratropical, lucidophyllous, and cloud forests, vary seasonally in 166 temperature and precipitation, but do not experience prolonged freezing temperatures 167 during the coldest months. Cold temperate forests also experience seasonal temperatures 168 and precipitation, but average minimum temperatures drop below freezing in at least one 169 of the coldest months.…”