Abstract
Host specialization after host shifting is traditionally viewed as the pathway to speciation in parasitic plants. However, geographical and environmental changes can also influence parasite speciation, through hybridization processes. Here we investigated the impact of past climatic fluctuations, environment, and host shifts on the genetic structure and patterns of hybridization and gene flow between Psittacanthus calyculatus and P. schiedeanus, a Mesoamerican species complex. Using microsatellites (408 individuals), we document moderate genetic diversity but high genetic differentiation between widespread parental clusters, calyculatus in dry pine-oak forests and schiedeanus in cloud forests. Bayesian analyses identified a third cluster, with admixture between parental clusters in areas of xeric and tropical dry forests and high levels of migration rates following secondary contact. Coincidently host associations in these areas differ from those in areas of parental species, suggesting that past hybridization played a role in environmental and host shifts. Overall, the observed genetic and geographic patterns suggest that these Psittacanthus populations could have entered a distinct evolutionary pathway. The results provide evidence for highlights on the importance of the Pleistocene climate changes, habitat differences, and potential host shifts in the evolutionary history of Neotropical mistletoes.
Highlights
The speciation process is viewed as a continuum with many stages that vary in space and time[1,2,3], for closely related taxa with varying levels of divergence[4]
The existence of two major clusters was supported by AMOVA, in which 5.8% of the total genetic variation was explained by significant differentiation between the CALY and SCHI genetic groups (Table S3)
We investigated patterns of genetic structure and levels of hybridization among groups of populations and estimated rates and directionality of migration over contemporary and historical timescales between P. calyculatus and P. schiedeanus using nuclear microsatellites
Summary
The speciation process is viewed as a continuum (the ‘speciation continuum’) with many stages that vary in space and time[1,2,3], for closely related taxa with varying levels of divergence[4]. Given that most avian seed dispersers and pollinators of loranth mistletoes are not sufficiently specialized[21], it is unlikely that gene dispersal vectors reproductively isolate mistletoes into populations growing on different hosts within a community (for alternative scenarios see[16,28,29]). Mistletoes are expected to establish and survive on higher-quality hosts (‘host quality’ hypothesis33) and, variation in host quality would account for non-random occurrence patterns of parasitic plants. Beyond these mechanisms determining the distribution at local and large geographical scales, the diversification of mistletoe species has been explained through different mechanisms linked to host-parasite interactions[12]. The geographic structuring of genetic variation in some mistletoe species has been explained as the result of past climate changes[31,32,37,38], landscape fragmentation[39], emergence of biogeographic barriers[30,31,32,38], and by the parasites’ own climatic niche preferences[40,41]
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