How ancient forest fragmentation and riparian connectivity generate high levels of genetic diversity in a microendemic Malagasy tree

  1. Jordi Salmona
  2. Axel Dresen
  3. Anicet E. Ranaivoson
  4. Sophie Manzi
  5. Barbara Le Pors
  6. Cynthia Hong‐Wa
  7. Jacqueline Razanatsoa
  8. Nicole V. Andriaholinirina
  9. Solofonirina Rasoloharijaona
  10. Marie‐Elodie Vavitsara
  11. Guillaume Besnard

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Abstract

Understanding landscape changes is central to predicting evolutionary trajectories and defining conservation practices. While human‐driven deforestation is intense throughout Madagascar, exceptions in areas such as the Loky‐Manambato region (north) raise questions regarding the causes and age of forest fragmentation. The Loky‐Manambato region also harbours a rich and endemic flora, whose evolutionary origin remains poorly understood. We assessed the genetic diversity of an endangered microendemic Malagasy olive species ( Noronhia spinifolia Hong‐Wa) to better understand the vegetation dynamics in the Loky‐Manambato region and its influence on past evolutionary processes. We characterized 72 individuals sampled across eight forests through nuclear and mitochondrial restriction‐associated DNA sequencing data and chloroplast microsatellites. Combined population and landscape genetics analyses indicate that N. spinifolia diversity is largely explained by the current forest cover, highlighting a long‐standing habitat mosaic in the region. This sustains a major and long‐term role of riparian corridors in maintaining connectivity across these antique mosaic habitats, calling for the study of organismal interactions that promote gene flow.

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  1. Version published to 10.1111/mec.16759
  2. Peer Community in Evolutionary Biology

    We currently live in the Anthropocene, the geological age characterized by a profound impact of human populations in the ecosystems and the environment. While there is little doubt about the action of humans in the shaping of present landscapes, it can be difficult to determine what the state of those landscapes was before humans started to modify them. This is the case of the Madagascar grasslands, whose origins have been debated with arguments proposing them either as anthropogenic, created with the arrival of humans around 2000BP, or as ancient features of the natural landscape with a forest fragmentation process due to environmental changes pre-dating human arrival [e.g. 1,2]. One way to clarify this question is through the genetic study of native species. Population continuity and fragmentation along time shape the structure of the genetic diversity in space. Species living in a uniform continuous habitat are expected to show genetic structuring determined only by geographical distance. Recent changes of the habitat can take many generations to reshape that genetic structure [3]. Thus, we expect genetic structure to reflect ancient features of the landscape.

    The work by Jordi Salmona and collaborators [4] studies the factors determining the population genetic structure of the Malagasy spiny olive (Noronhia spinifolia). This narrow endemic species is distributed in the discontinuous forest patches of the Loky-Manambato region (northern Madagascar). Jordi Salmona and collaborators genotyped 72 individuals distributed across the species distribution with restriction associated DNA sequencing and organelle microsatellite markers. Then, they studied the population genetic structure of the species. Using isolation-by-resistance models [5], they tested the influence of several landscape features (forest cover, roads, rivers, slope, etc.) on the connectivity between populations. Maternally inherited loci (chloroplast and mitochondria) and bi-parentally inherited loci (nuclear), were analysed separately in an attempt to identify the role of pollen and seed dispersal in the connectivity of populations.

    Despite the small distribution of the species, Jordi Salmona and collaborators [4] found remarkable levels of genetic diversity. The spatial structure of this diversity was found to be mainly explained by the forest cover of the landscape, suggesting that the landscape has been composed by patches of forests and grasslands for a long time. The main role of forest cover for the connectivity among populations also highlights the importance of riparian forest as dispersal corridors. Finally, differences between organelle and nuclear markers were not enough to establish any strong conclusion about the differences between pollen and seed dispersal.

    The results presented by Jordi Salmona and collaborators [4] contribute to the understanding of the history and ecology of understudied Madagascar ecosystems. Previous population genetic studies  in some forest-dwelling mammals have been interpreted as supporting an old age for the fragmented landscapes in northern Madagascar [e.g. 1,6]. To my knowledge, this is the first study on a tree species. While this work might not completely settle the debate, it emphasizes the importance of studying a diversity of species to understand the biogeographic dynamics of a region.

    References

    1. Quéméré, E., X. Amelot, J. Pierson, B. Crouau-Roy, L. Chikhi (2012) Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region. Proceedings of the National Academy of Sciences of the United States of
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  3. Version published to 10.1101/2020.11.25.394544 on bioRxiv