Fine‐scale spatial genetic structure, mating, and gene dispersal patterns in Parkia biglobosa populations with different levels of habitat fragmentation

Abstract

Premise A good understanding of genetic variation and gene dispersal in tree populations is crucial for their sustainable management, particularly in a context of rapid environmental changes. West African Sudanian savannahs are being fragmented and degraded, partly due to expansion of crop cultivation and monocultures that reduce tree density and may impact pollinators. The population dynamics of important indigenous trees could also be affected. We investigated the influence of habitat fragmentation on patterns of genetic diversity and gene dispersal of a key Sudanian agroforestry tree species, Parkia biglobosa . Methods Using 10 highly polymorphic nuclear microsatellites, we genotyped 2475 samples from reproductive trees, seedlings, and embryos in four tree populations presenting different levels of habitat fragmentation. Results Parkia biglobosa presented similar high genetic diversity across the four populations studied. Genetic diversity and inbreeding were similar between adults and embryo cohorts. In all four populations, the selfing rate was less than 1%. The effective number of pollen donors per tree was high ( N EP ~ 18–22), as was the pollen immigration rate (from 34 to 74%). Pollen dispersal was characterized by a fat‐tailed distribution with mean estimates exceeding 200 m. In three populations, stem diameter had a pronounced effect on male reproductive success. Here, the highest male reproductive success was observed in trees with a diameter at breast height between 60 and 75 cm. Conclusions At the scale analyzed, fragmentation does not seem to pose limitations to gene flow in any of the sites investigated, regardless of the landscape configuration associated with the different tree stands. The study provides useful insights on the reproductive biology of an important tree species in the West African savannahs.

Depicting the mating system and patterns of contemporary pollen flow in trees of the genus Anadenanthera (Fabaceae)

“…Although we have not investigated the spatial genetic structure in these populations due to the small sample sizes mainly for A. colubrina , it can be inferred based on the occurrence of pollen flow over relatively short distances and the biparental inbreeding observed in the studied populations. These results are consistent with other tree species in fragmented populations that have shown elevated levels of mating between related individuals ( Ismail et al, 2012 ; Tambarussi et al, 2017 ; Souza et al, 2018 ) and inbreeding ( Fuchs, Lobo & Quesada, 2003 ; Jump & Peñuelas, 2006 ; Kettle et al, 2007 ; Dick et al, 2008 ; Vranckx et al, 2011 ; Zhang et al, 2012 ; Finger et al, 2014 ; Tambarussi et al, 2017 ; Seoane et al, 2019 ; but see Lompo et al, 2020 ). Such findings could be explained by the genetic structure of natural clusters (i.e., angicais ) in the parental generation, with near-neighbor related trees resulting from seed dispersal close to the seed-tree (autochoric dispersion), profuse flowering, and pollinator behavior.…”

“…Gene flow by pollen dispersal outside the boundaries of forest fragments has been reported for several animal-pollinated plant species ( Nason & Hamrick, 1997 ; Sato et al, 2006 ; Nazareno & Carvalho, 2009 ; Ottewell et al, 2012 ; Côrtes et al, 2013 ; Saro et al, 2014 ; Guidugli et al, 2016 ; Garcia et al, 2019 ; Skogen et al, 2019 ; Lompo et al, 2020 ). Even in an extremely fragmented landscape, such as the Ribeirão Preto region, we observed a moderate frequency (30–35%) of pollen immigration for both Anadenanthera species, showing that pollen flow outside the edges of small forest fragments is feasible.…”

“…As an illustrative example, in the same fragmented landscape where Adenanthera species occurs, a gene flow study involving the allogamous species Carianiana estrellensis (Lecythidaceae) revealed a lack of inbreeding as a consequence of extensive gene immigration and high outcrossing rates ( Guidugli et al, 2016 ). Therefore, to formulate biological diversity conservation policies and management programs, mainly in fragmented landscapes, an understanding of the mating system parameters (e.g., outcrossing, selfing and biparental inbreeding rates) in addition to estimates of contemporary gene flow in plant populations are indispensable (e.g., Allard, 1999 ; Finkeldey, 2005 ; Guidugli et al, 2016 ; Zhang et al, 2019 ; Lompo et al, 2020 ).…”

There Is No ‘Rule of Thumb’: Genomic Filter Settings for a Small Plant Population to Obtain Unbiased Gene Flow Estimates

“…Indeed, even in the highly fragmented landscape that D. jueirana-facao inhabits, we observed a moderate frequency (31.25%) of gene immigration, indicating that pollen movement beyond the edges of the small fragment may reach distances of 12 km (i.e., there is long-distance pollen dispersal between the forest fragment and the nearest pollen source). Gene flow by pollen dispersal beyond the edges of seemingly isolated forest fragments has been documented for distinct tree species, including species that are animal-pollinated (e.g., Nason and Hamrick, 1997 ; Sato et al, 2006 ; Nazareno and Carvalho, 2009 ; Ottewell et al, 2012 ; Côrtes et al, 2013 ; Saro et al, 2014 ; Guidugli et al, 2016 ; Garcia et al, 2019 ; Skogen et al, 2019 ; Lompo et al, 2020 ). Our result suggests that the open landscape due to deforestation, where the small population of D. jueirana-facao are located, facilitates pollen flow and may ameliorate the expected detrimental genetic effects of forest fragmentation.…”

The Future of Food: Domestication and Commercialization of Indigenous Food Crops in Africa over the Third Decade (2012–2021)

“…Despite the importance of this long history and its associated good management practices, the rich forest biodiversity in the region is threatened by changes in land use and climate change. The two factors are implicated in habitat fragmentation and/or the contraction of suitable habitat of indigenous trees such as tamarind (Tamarindus indica) [160], Detarium microcarpum [399], V. paradoxa [124], and P. biglobosa [400]. This is threatening millions of livelihoods that depend on these natural resources.…”