Introduction
Seed plant populations may be linked through two key ecological
processes: pollen and seed dispersal (Krauss et al. 2008,
Ballesteros-Mejia et al. 2016, Gelmi-Candusso et al. 2017, Cortés et al.
2018). Pollen dispersal by animals in particular is considered as major
driver of plant population structure, often more important than seed
dispersal (Yu et al. 2010, Clavino-Cancela et al. 2012, Kartzinel et al.
2013, Skogen et al. 2019, Gamba & Muchhala 2020, Nazareno et al. 2021).
Animal pollinators differ markedly in their mobility, flower-visitation
behaviour and rates of pollen transfer (Bawa 1992, Breed et al. 2015,
Krauss et al. 2017, Dellinger et al. 2021). These differences may result
in distinct within-population mating patterns and among-population
differentiation (Wessinger 2021). Less mobile pollinators (i.e. small
insects, territorial hummingbirds) may generate localized mating
patterns between neighbouring individuals, increased inbreeding, and
high population differentiation (Schoen & Clegg 1984, Opedal et al.
2017, Schmidt-Lebuhn et al. 2019, Wessinger 2021). Highly mobile
pollinators (i.e. flying vertebrates, large bees), in contrast, may
promote outcrossing and gene flow over larger geographic distances
(Hughes et al. 2007, Whelan et al. 2009, Ballesteros-Mejia et al. 2016,
Gamba & Muchhala 2020). Understanding the extent to which different
animal pollinators drive genetic differentiation, ultimately affecting
the potential for adaptive evolution and speciation, is essential for
better resolving macroevolutionary processes of angiosperm
diversification, but it is also of major relevance for choosing
appropriate management strategies in human-altered landscapes and under
current climate change (Hadley et al. 2012, Toon et al. 2014, Castilla
et al. 2017). Surprisingly, however, the impact of different pollination
strategies on population genetic parameters across related plant species
(accounting for shared macroevolutionary background) has rarely been
assessed (Barbará et al. 2007, Kramer et al. 2011).
Besides (pollinator-mediated) gene flow, a species’ present-day
population genetic structure may be influenced by climatic and
demographic history, landscape features, and adaptation to distinct (and
changing) abiotic environmental conditions (Helmstetter et al. 2020).
Mountains in particular, with their highly heterogeneous, rugged
terrain, create dispersal barriers and strong environmental gradients
across small spatial and temporal scales, reinforcing population
differentiation and, potentially, speciation (Kisel & Barraclough 2010,
Surget-Groba & Kay 2013, Nevado et al. 2019). Accordingly, mountains
across the world represent biodiversity hotspots with an exceptional
number of recent (plant) radiations (Luebert & Weigend 2014, Rahbek et
al. 2018, Rangel et al. 2018). Several of these radiations coincide with
phases of mountain uplift or Pleistocene glacial cycles (Cortés et al.
2018). Particularly the latter, inducing repeated periods of population
isolation, range shifts and habitat recolonization, have left imprints
in the current population genetic structure (Ornelas et al. 2013, Ortego
et al. 2014, Escobar et al. 2020).
The tropical Andes represent one of the planet’s biodiversity hotspots,
encompassing lowland rainforests, montane cloud forests and Páramo
grasslands (Gentry 1982). The effects of Pleistocene climatic
fluctuations in these habitats are complex, with idiosyncratic responses
documented among different groups of organisms and geographic regions
(Ramírez-Barahona & Eguiarte 2013, Vasconcellos et al. 2019). Some
studies suggest that (cloud) forests were fragmented into small refugia
at mid elevations during dry glacial periods, leading to marked
population structuring and a loss of genetic diversity (‘dry-refugia
hypothesis’, Haffer 1969, Gutíerrez-Rodríguez et al. 2011). Other data
indicate that Neotropical mountains remained moist, with a mere downward
and consecutive upward migration of forest zones, resulting in diffuse
population structuring and increased genetic diversity in continuously
forested areas (e.g. Colombian Chocó; ‘moist-forest hypothesis’,
Carnaval et al. 2009, Valencia et al. 2010, Ornelas et al. 2019,
Hernández-Langford et al. 2020).
Clearly, with their vital role in mediating gene flow, pollinators
differing in mobility have the capacity of exponentiating or offsetting
isolating effects of geographic or climatic barriers. Importantly,
pollinators are not independent of their abiotic environment either. The
flower visitation activity of ectothermic insect pollinators in
particular may be strongly reduced by adverse weather conditions
prevalent in tropical mountains, while endothermic vertebrates are less
affected by weather fluctuations (Cruden 1972, Dellinger et al. 2021).
To date, however, we largely lack studies from related Neotropical
plants differing in pollination strategy to evaluate the relative
contributions of biotic interactions, the (current and historic) abiotic
environment, and landscape features to structuring population genetic
diversity. Connecting these factors, however, will ultimately improve
our understanding of the microevolutionary dynamics underlying
(Neo)tropical diversity.
Here, we explore the effects of multifarious factors (geographic
distance, topography, habitat suitability, Pleistocene climatic
instability, environment) on population genomic diversity and
differentiation across six related Neotropical plant species
(Merianieae, Melastomataceae) differing in pollination strategy (but not
in seed dispersal, see Material and Methods). We aim to understand
whether mating patterns are more localized (i.e. lower heterozygosity
and nucleotide diversity, higher inbreeding, stronger within-population
isolation-by-distance) in localities of bee-pollinated species (two
species) than of vertebrate-pollinated species (four species), and
whether flying vertebrate pollinators consistently promote higher levels
of gene flow across larger (geographical, environmental) distances than
bees. We further expect stronger effects of variation in climatic
conditions in bee- than in vertebrate-pollinated species given the
strong link between abiotic conditions and the activity of ectothermic
insect pollinators. For each species, we contrast two adjacent
(< 12 km) localities against three to four more distant
localities and directly address differences in distribution ranges and
ecosystems colonized through niche modelling approaches.