Plants, as sessile organisms, depend on seed dispersal as a crucial mechanism for colonizing new areas. This has driven the evolution of various dispersal strategies in plants, including the development of ‘megafruits’—fruits typically larger than 4 cm containing up to 5 large seeds. Megafruits are thought to have evolved primarily for dispersal by megafauna, the largest animals in an ecosystem, which includes fruit-eaters capable of transporting seeds across vast distances, known as ‘megafrugivores’. Such interactions were crucial for maintaining connectivity among plant populations over large distances. However, most megafauna disappeared during the Late Pleistocene, largely due to human activities.
Madagascar, once home to a diverse megafrugivore assemblage such as giant lemurs, elephant birds and giant tortoises, presents an ideal setting to study these past interactions. The extinction of these creatures around 1,000 years ago, poses intriguing questions about the ongoing impact on plant populations, especially in the context of their role in seed dispersal of plants with megafruits.
Hypothetical past Madagascar when megafrugivores such as giant lemurs, elephant birds and giant tortoises were still probably providing long-dispersal events for plants with megafruits. Around 1,000 years ago, human impact largely drove all megafrugivores to extinction in Madagascar. Such historical interactions with now extinct megafrugivores may have left imprints on current species and populations genetics. See the whole video here: https://www.tricklabor.com/en/portfolio/madagascars-megafauna/
Fieldwork in Madagascar
Local botanist Tahina Razafindrahaja holding a rotting megafruit from the palm species Borassus madagascariensis. This is the palm species in Madagascar bearing the largest fruits (30 cm average fruit length), which are not dispersed by any known extant frugivore and they are normally found rotting on the ground.
To investigate the consequences of the extinction of megafrugivores on plants bearing megafruits, I travelled to Madagascar in the summer of 2019. There, I was warmly welcomed by the local team of the Kew Madagascar Conservation Centre (KMCC), who became my family for the next 3 months. We collected samples from Malagasy palms (the family of plants in Madagascar with most species bearing megafruits), specially on the western part of Madagascar, where megafrugivores were historically prevalent, and where the current distribution of palms still shows imprints from the past distribution of megafrugivores.
We collected DNA from four Malagasy palm species dispersed by animals, categorized into three fruit size classes: the large megafruited palm (Borassus madagascariensis, 30 cm average length), medium-sized megafruited palms (Hyphaene coriacea, 5.5 cm; Bismarckia nobilis, 4.4 cm), and a small-fruited palm (Chrysalidocarpus madagascariensis, 1.3 cm).
Our study
Back at the iDiv research institute in Leipzig, Germany, where I was doing my doctoral studies at that time at Renske E. Onstein’s lab, I extracted DNA and we generated double-digest restriction-site-associated DNA sequencing data for these palms. With these data, we assessed the genetic differentiation and recent migration among populations of the four animal-dispersed palm species. We integrated that with (past) distribution ranges for extinct and extant seed-dispersing animals, landscape and human impact data, and applied linear mixed-effects models to explore the drivers of genetic variation in these palms.
Pictures from fieldwork and the awesome team that made everything possible! Upper left picture: From left to right, co-author of the paper and local botanist Vonona Randrianasolo, local botanist Henintsoa Razanajatovo and me posing proudly in front of Borassus madagascariensis. Lower left picture: Local botanist Fidelis Randrianasolo, most awesome KMCC driver Roger Rajaonarison, me and local botanists Tahina Razafindrahaja and Andry Rakotoarisoa. Right picture: Vonona Randrianasolo sampling the not-so-easy to sample B. madagascariensis. Want to see more? Here is a video about my fieldwork in Madagascar: https://youtu.be/pBEHnJQBH9U?si=p0kJrvEwgw0ovyIk
Our findings
Our results showed that palm populations that historically shared more megafrugivore species had lower genetic differentiation, suggesting that megafrugivore-mediated seed dispersal in the past promoted gene flow among populations. In comparison, the impact of existing frugivore diversity on genetic differentiation was only evident in the small-fruited palm species. Moreover, landscape connectivity (environmental suitability, forest cover and river density) and human impact (road density), also lowered genetic differentiation, indicating that even after the extinction of megafrugivores, other dispersal methods (like human or river-mediated dispersal) may have played roles in maintaining low genetic differentiation among populations of megafruited palms. Our study illustrates how species interactions that occurred over a millennium ago can leave imprints on population genetics.
Read the full piece on the Journal of Ecology entitled: ‘Genomic signatures of past megafrugivore-mediated dispersal in Malagasy palms’
Follow the authors on X here: @LauraMendezCue; @renskeonstein; @DurkaWalter; @w_eiserhardt; @BillJBaker, @vononarbgkew1; @TeamKMCC; @idiv
