Abstract

Restricted gene flow may lead to the loss of genetic diversity and higher genetic differentiation among populations, but the genetic consequences of megafauna extinction for plant populations still remain to be assessed. We performed a phylogenetic-independent meta-analysis across 102 Neotropical plants to test the hypothesis that plant species with megafaunal seed dispersal syndrome have a lower genetic diversity and a higher genetic differentiation than those without it. We classified as megafauna-dependent plant species those that potentially relied only on megafauna to seed dispersal, and as megafauna-independent those that relied on megafauna and other seed dispersers. Our data comprised 98 studies using microsatellite markers. We found no statistical difference in genetic diversity and differentiation between plants with megafauna and non-megafauna seed dispersal syndrome, although the statistical power to detect differences in genetic differentiation was low. Moreover, we found no statistical difference between megafauna-dependent and megafauna-independent plant species. We then used generalized linear mixed models and phylogenetic generalized least square models to investigate the effects of megafaunal seed dispersal syndromes and reproductive traits on variation in genetic diversity and genetic differentiation. We found no effect of megafaunal syndrome, rather, reproductive traits, such as pollination mode, mating, and breeding systems, showed significant effects. Our findings show that the genetic studies of Neotropical plants performed so far show no difference in genetic diversity and differentiation in plants with megafaunal compared to those with non-megafaunal seed dispersal syndromes. Our results also provide evidence pointing out that plant species with megafaunal seed dispersal syndromes may have used different strategies to counterbalance the extinction of their mutualistic megafauna dispersers, such as the dispersal by extant mammals that may promote long-distance seed dispersal. Our results also reinforce the importance of pollination to long-distance gene flow in Neotropical plants.

Highlights

  • Neotropical plants producing large fruits and seeds or seeds with thick and hard endocarps or coats embedded in indehiscent fruits are known as biological anachronisms (Janzen and Martin, 1982), adapted to a extinct megafauna that once dominated Pleistocene Neotropical landscapes

  • Power analysis indicates that results for genetic diversity parameters (He and allelic richness (AR)) have enough statistical power (Tables S3–S5) to support results of the meta-analysis

  • Our findings show no significant signal of megafauna extinction in genetic diversity and differentiation of Neotropical plants

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Summary

Introduction

Neotropical plants producing large fruits and seeds or seeds with thick and hard endocarps or coats embedded in indehiscent fruits are known as biological anachronisms (Janzen and Martin, 1982), adapted to a extinct megafauna (mammals >1,000 kg) that once dominated Pleistocene Neotropical landscapes. Megafauna species may have promoted long-distance dispersal by massive seed dispersal (Pires et al, 2017), that is, defecating large amounts of seeds over large areas, or by carrying large individual seeds over long distances (Janzen and Martin, 1982; Guimarães et al, 2008; Hansen and Galetti, 2009; Pires et al, 2017). In the Neotropics, fruits of megafauna syndrome species are consumed by many extant mammals, such as agouti, but only extant large mammals, such as tapirs, large bats, Atelinae monkeys, manned wolf, and deer, can act as long-distance seed dispersers by endozoochory (Tabarelli and Peres, 2002; Guimarães et al, 2008; Hansen and Galetti, 2009). Germination rates of seeds swallowed and defecated by larger mammals may be higher than those of seeds consumed by smaller mammals because of greater scarification (Westoby et al, 1996; Moles and Westoby, 2004; Bodmer and Ward, 2006)

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