Population structure in Neotropical plants: Integrating pollination biology, topography and climatic niches

Abstract

Animal pollinators mediate gene flow among plant populations, but in contrast to well‐studied topographic and (Pleistocene) environmental isolating barriers, their impact on population genetic differentiation remains largely unexplored. Comparing how these multifarious factors drive microevolutionary histories is, however, crucial for better resolving macroevolutionary patterns of plant diversification. Here we combined genomic analyses with landscape genetics and niche modelling across six related Neotropical plant species (424 individuals across 33 localities) differing in pollination strategy to test the hypothesis that highly mobile (vertebrate) pollinators more effectively link isolated localities than less mobile (bee) pollinators. We found consistently higher genetic differentiation (FST) among localities of bee‐ than vertebrate‐pollinated species with increasing geographical distance, topographic barriers and historical climatic instability. High admixture among montane populations further suggested relative climatic stability of Neotropical montane forests during the Pleistocene. Overall, our results indicate that pollinators may differentially impact the potential for allopatric speciation, thereby critically influencing diversification histories at macroevolutionary scales.

Pollinator type strongly impacts gene flow within and among plant populations for six Neotropical species

“…Pollinators with large foraging areas can carry pollen long distances, potentially enhancing gene flow within and among plant populations, while pollinators with local foraging behavior may reduce gene flow. This trend has been predicted in seminal reviews (Levin, 1981;Loveless & Hamrick, 1984), and supported in empirical studies of temperate and subtropical plants (Breed et al, 2015;Kramer et al, 2011;Linhart et al, 1987;Linhart & Grant, 1996), and in a recent study in a set of neotropical Merianieae (Dellinger et al, 2022).…”

“…The contrasting effect of different pollinators on plant gene flow has remained largely unexplored, especially in the Neotropics (Wessinger, 2021, but please refer to Dellinger et al, 2022). Our study highlights that pollinator type can have a strong impact on genetic structure: among our species pairs, two of the three species pollinated by insects had greater levels of population genetic differentiation and stronger FSGS than their hummingbird‐pollinated counterparts (Tables 2 and 3, Figure 1).…”

“…Our results also suggest that large insects, such as euglossine bees, can connect plant populations as effectively as traplining hummingbirds. Therefore, the effect of different animal pollinators on neotropical plant gene flow can be significantly different at local (within populations) and regional (among populations) scales (e.g., Dellinger et al, 2022). Our results are also relevant to conservation efforts, suggesting that plants pollinated by small insects are likely to be very susceptible to habitat fragmentation (more so than vertebrate-pollinated plants, e.g., Côrtes et al, 2013), as this can further isolate populations and result in the loss of genetic variability due to increased genetic drift (Aguilar et al, 2008(Aguilar et al, , 2019.…”

Evolutionary convergence on hummingbird pollination in Neotropical Costus provides insight into the causes of pollinator shifts

“…Previous studies of Costus pollination found higher visitation rates by bees but did not examine pollen transfer efficiency or pollen quality (Kay & Schemske, 2003 ). Other studies have found more extensive gene flow in vertebrate‐pollinated compared to bee‐pollinated plants (Krauss et al ., 2017 ; Dellinger et al ., 2022b ). Outcrossing via hummingbirds could benefit Costus species, which, although self‐compatible, have substantial heterozygosity and inbreeding depression (Schemske, 1983 ; Surget‐Groba & Kay, 2013 ).…”

The genetic mechanisms underlying the convergent evolution of pollination syndromes in the Neotropical radiation of Costus L.

“…Beyond looking at selection across individual genes, recent studies have shown evidence of genomic-level changes being driven explicitly by associations with pollinators; examples include higher genetic differentiation (F ST ) in bee vs. vertebrate pollinated populations with increased geographic distance ( Dellinger et al, 2022 ), and observed allele frequency changes following generations of bumble bee pollinated treatments when compared with the control ( Frachon and Schiestl, 2021 ). Additionally, linkage disequilibrium (LD) has been observed to decay more rapidly with higher rates of outcrossing due to increased effective recombination ( Morrell et al, 2005 ; Zhu et al, 2016 ), with self-incompatibility (i.e., forced outcrossing) leading to even more rapid decay as observed in the tea plant ( Camellia sinensis [L.] Kuntze; Theaceae; Niu et al, 2019 ).…”