Long-distance pollen and seed dispersal and inbreeding depression in Hymenaea stigonocarpa (Fabaceae: Caesalpinioideae) in the Brazilian savannah.

Marcela A Moraes,Alexandre M Sebbenn,Miguel L M Freitas,Mario L T Moraes,Celso L Marino,Alexandre M Da Silva,Bruno C Rossini,Jose Cambuim,Thaisa Y K Kubota

doi:10.1002/ece3.4253

Marcela A Moraes, Alexandre M Sebbenn + Show 7 more

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https://doi.org/10.1002/ece3.4253

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Abstract

Hymenaea stigonocarpa is a neotropical tree that is economically important due to its high‐quality wood; however, because it has been exploited extensively, it is currently considered threatened. Microsatellite loci were used to investigate the pollen and seed dispersal, mating patterns, spatial genetic structure (SGS), genetic diversity, and inbreeding depression in H. stigonocarpa adults, juveniles, and open‐pollinated seeds, which were sampled from isolated trees in a pasture and trees within a forest fragment in the Brazilian savannah. We found that the species presented a mixed mating system, with population and individual variations in the outcrossing rate (0.53–1.0). The studied populations were not genetically isolated due to pollen and seed flow between the studied populations and between the populations and individuals located outside of the study area. Pollen and seed dispersal occurred over long distances (>8 km); however, the dispersal patterns were isolated by distance, with a high frequency of mating occurring between near‐neighbor trees and seeds dispersed near the parent trees. The correlated mating for individual seed trees was higher within than among fruits, indicating that fruits present a high proportion of full‐sibs. Genetic diversity and SGS were similar among the populations, but offspring showed evidence of inbreeding, mainly originating from mating among related trees, which suggests inbreeding depression between the seed and adult stages. Selfing resulted in a higher inbreeding depression than mating among relatives, as assessed through survival and height. As the populations are not genetically isolated, both are important targets for in situ conservation to maintain their genetic diversity; for ex situ conservation, seeds can be collected from at least 78 trees in both populations separated by at least 250 m.

Highlights

Tropical forests around the world have experienced extensive fragmentation, resulting in tree populations that are spatially isolated in small forest fragments and individuals scattered throughout landscapes interspersed with pastures, agricultural areas, highways, and cities
Due to the fact that in the São Paulo and Mato Grosso do Sul states, H. stigonocarpa is currently only found in forest fragments and as isolated trees in pastures, we investigated the effects of forest fragmentation on the genetic structure of two of the remaining populations in this region, where the species populations that remain are not continued in natural forests and are only found in fragmented populations
We addressed the following questions: (a) Is there gene flow between the pasture and the forest fragment? (b) What are the distance and patterns of pollen and seed dispersal in the populations? (c) Are there differences in the rates of selfing and mating among relatives, and is there a paternity correlation between trees in the pasture and the forest fragment? (d) Is the paternity correlation lower among fruits than within fruits? (e) Are the levels of effective size variance lower and inbreeding higher in open-pollinated seeds collected from the pasture than in seeds collected from trees in the forest fragment? (f) Do selfing and mating among related trees produce inbreeding depression?

Summary

| INTRODUCTION

Tropical forests around the world have experienced extensive fragmentation, resulting in tree populations that are spatially isolated in small forest fragments and individuals scattered throughout landscapes interspersed with pastures, agricultural areas, highways, and cities. Parentage analysis (paternity and maternity) has been used extensively to study gene dispersal in tree populations in a wide range of environments, including continuous, fragmented, and logged forests, isolated trees in pastures, and seed orchards (Burczyk, DiFazio & Adams, 2004; Ellstrand, 2014; Oddou-Muratorio & Klein, 2008; Smouse & Sork, 2004) In such analyses, it is important to differentiate between the realized and effective gene flow because deterministic factors such as natural selection and stochastic factors such as random mortality, predation, and disease can come into play between the seed and juvenile (regenerant) stages, and many seeds never reach the juvenile and/or adult stages. We addressed the following questions: (a) Is there gene flow between the pasture and the forest fragment? (b) What are the distance and patterns of pollen and seed dispersal in the populations? (c) Are there differences in the rates of selfing and mating among relatives, and is there a paternity correlation between trees in the pasture and the forest fragment? (d) Is the paternity correlation lower among fruits than within fruits? (e) Are the levels of effective size variance lower and inbreeding higher in open-pollinated seeds collected from the pasture than in seeds collected from trees in the forest fragment? (f) Do selfing and mating among related trees produce inbreeding depression?

| MATERIALS AND METHODS

Findings

| DISCUSSION