Genomic signatures of past megafrugivore-mediated dispersal in Malagasy palms

Laura Méndez; Christopher D. Barratt; Walter Durka; W. Daniel Kissling; Wolf L. Eiserhardt; William J. Baker; Vonona Randrianasolo; Renske E. Onstein

doi:10.1111/1365-2745.14340

Genomic signatures of past megafrugivore-mediated dispersal in Malagasy palms

Laura Méndez^*, Christopher D. Barratt, Walter Durka, W. Daniel Kissling, Wolf L. Eiserhardt, William J. Baker, Vonona Randrianasolo, Renske E. Onstein

^*Corresponding author af dette arbejde

Institut for Biologi - Økoinformatik og biodiversitet

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

Abstract

Seed dispersal affects gene flow and hence genetic differentiation of plant populations. During the Late Quaternary, most fruit-eating and seed-dispersing megafauna went extinct, but whether these animals have left signatures in the population genetics of their food plants, particularly those with large, ‘megafaunal’ fruits (i.e. >4 cm—megafruits), remains unclear. Here, we assessed the population history, genetic differentiation and recent migration among populations of four animal-dispersed palm (Arecaceae) species with large (Borassus madagascariensis), medium-sized (Hyphaene coriacea, Bismarckia nobilis) and small (Chrysalidocarpus madagascariensis) fruits on Madagascar. We integrated double-digest restriction-site-associated DNA sequencing (ddRAD) of 167 individuals from 25 populations with (past) distribution ranges for extinct (e.g., giant lemurs and elephant birds) and extant seed-dispersing animals, landscape and human impact data, and applied linear mixed-effects models to explore the drivers of genetic variation in Malagasy palms. Palm populations that shared more megafrugivore species in the past had lower genetic differentiation than populations that shared fewer megafrugivore species. This suggests that megafrugivore-mediated seed dispersal in the past may have led to frequent gene flow among populations. In comparison, extant frugivore diversity only decreased genetic differentiation in the small-fruited palm. Furthermore, genetic differentiation of all palm species decreased with landscape connectivity (i.e. environmental suitability, forest cover and river density) and human impact (i.e. road density), while migration rates of the small-fruit palm increased with road density. Synthesis. Our results suggest that the legacy of megafrugivores regularly achieving long dispersal distances is still reflected in the population genetics of palms that were formerly dispersed by such animals. Furthermore, low genetic differentiation was possibly maintained after the megafauna extinctions through alternative dispersal (e.g. human- or river-mediated), long generation times and long lifespans of these megafruit palms. Our study illustrates how species interactions that happened >1000 years ago can leave imprints in their population genetics.

Originalsprog	Engelsk
Tidsskrift	Journal of Ecology
Vol/bind	112
Nummer	7
Sider (fra-til)	1583-1598
Antal sider	16
ISSN	0022-0477
DOI	https://doi.org/10.1111/1365-2745.14340
Status	Udgivet - jul. 2024

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@article{2dc284f04a0d4ee6890d491f37751103,

title = "Genomic signatures of past megafrugivore-mediated dispersal in Malagasy palms",

abstract = "Seed dispersal affects gene flow and hence genetic differentiation of plant populations. During the Late Quaternary, most fruit-eating and seed-dispersing megafauna went extinct, but whether these animals have left signatures in the population genetics of their food plants, particularly those with large, {\textquoteleft}megafaunal{\textquoteright} fruits (i.e. >4 cm—megafruits), remains unclear. Here, we assessed the population history, genetic differentiation and recent migration among populations of four animal-dispersed palm (Arecaceae) species with large (Borassus madagascariensis), medium-sized (Hyphaene coriacea, Bismarckia nobilis) and small (Chrysalidocarpus madagascariensis) fruits on Madagascar. We integrated double-digest restriction-site-associated DNA sequencing (ddRAD) of 167 individuals from 25 populations with (past) distribution ranges for extinct (e.g., giant lemurs and elephant birds) and extant seed-dispersing animals, landscape and human impact data, and applied linear mixed-effects models to explore the drivers of genetic variation in Malagasy palms. Palm populations that shared more megafrugivore species in the past had lower genetic differentiation than populations that shared fewer megafrugivore species. This suggests that megafrugivore-mediated seed dispersal in the past may have led to frequent gene flow among populations. In comparison, extant frugivore diversity only decreased genetic differentiation in the small-fruited palm. Furthermore, genetic differentiation of all palm species decreased with landscape connectivity (i.e. environmental suitability, forest cover and river density) and human impact (i.e. road density), while migration rates of the small-fruit palm increased with road density. Synthesis. Our results suggest that the legacy of megafrugivores regularly achieving long dispersal distances is still reflected in the population genetics of palms that were formerly dispersed by such animals. Furthermore, low genetic differentiation was possibly maintained after the megafauna extinctions through alternative dispersal (e.g. human- or river-mediated), long generation times and long lifespans of these megafruit palms. Our study illustrates how species interactions that happened >1000 years ago can leave imprints in their population genetics.",

keywords = "Arecaceae, ddRAD, genetic differentiation, megafauna extinction, population genomics, recent migration rate, seed dispersal",

author = "Laura M{\'e}ndez and Barratt, {Christopher D.} and Walter Durka and Kissling, {W. Daniel} and Eiserhardt, {Wolf L.} and Baker, {William J.} and Vonona Randrianasolo and Onstein, {Renske E.}",

note = "Publisher Copyright: {\textcopyright} 2024 The Authors. Journal of Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.",

year = "2024",

month = jul,

doi = "10.1111/1365-2745.14340",

language = "English",

volume = "112",

pages = "1583--1598",

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issn = "0022-0477",

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T1 - Genomic signatures of past megafrugivore-mediated dispersal in Malagasy palms

AU - Méndez, Laura

AU - Barratt, Christopher D.

AU - Durka, Walter

AU - Kissling, W. Daniel

AU - Eiserhardt, Wolf L.

AU - Baker, William J.

AU - Randrianasolo, Vonona

AU - Onstein, Renske E.

PY - 2024/7

Y1 - 2024/7

N2 - Seed dispersal affects gene flow and hence genetic differentiation of plant populations. During the Late Quaternary, most fruit-eating and seed-dispersing megafauna went extinct, but whether these animals have left signatures in the population genetics of their food plants, particularly those with large, ‘megafaunal’ fruits (i.e. >4 cm—megafruits), remains unclear. Here, we assessed the population history, genetic differentiation and recent migration among populations of four animal-dispersed palm (Arecaceae) species with large (Borassus madagascariensis), medium-sized (Hyphaene coriacea, Bismarckia nobilis) and small (Chrysalidocarpus madagascariensis) fruits on Madagascar. We integrated double-digest restriction-site-associated DNA sequencing (ddRAD) of 167 individuals from 25 populations with (past) distribution ranges for extinct (e.g., giant lemurs and elephant birds) and extant seed-dispersing animals, landscape and human impact data, and applied linear mixed-effects models to explore the drivers of genetic variation in Malagasy palms. Palm populations that shared more megafrugivore species in the past had lower genetic differentiation than populations that shared fewer megafrugivore species. This suggests that megafrugivore-mediated seed dispersal in the past may have led to frequent gene flow among populations. In comparison, extant frugivore diversity only decreased genetic differentiation in the small-fruited palm. Furthermore, genetic differentiation of all palm species decreased with landscape connectivity (i.e. environmental suitability, forest cover and river density) and human impact (i.e. road density), while migration rates of the small-fruit palm increased with road density. Synthesis. Our results suggest that the legacy of megafrugivores regularly achieving long dispersal distances is still reflected in the population genetics of palms that were formerly dispersed by such animals. Furthermore, low genetic differentiation was possibly maintained after the megafauna extinctions through alternative dispersal (e.g. human- or river-mediated), long generation times and long lifespans of these megafruit palms. Our study illustrates how species interactions that happened >1000 years ago can leave imprints in their population genetics.

AB - Seed dispersal affects gene flow and hence genetic differentiation of plant populations. During the Late Quaternary, most fruit-eating and seed-dispersing megafauna went extinct, but whether these animals have left signatures in the population genetics of their food plants, particularly those with large, ‘megafaunal’ fruits (i.e. >4 cm—megafruits), remains unclear. Here, we assessed the population history, genetic differentiation and recent migration among populations of four animal-dispersed palm (Arecaceae) species with large (Borassus madagascariensis), medium-sized (Hyphaene coriacea, Bismarckia nobilis) and small (Chrysalidocarpus madagascariensis) fruits on Madagascar. We integrated double-digest restriction-site-associated DNA sequencing (ddRAD) of 167 individuals from 25 populations with (past) distribution ranges for extinct (e.g., giant lemurs and elephant birds) and extant seed-dispersing animals, landscape and human impact data, and applied linear mixed-effects models to explore the drivers of genetic variation in Malagasy palms. Palm populations that shared more megafrugivore species in the past had lower genetic differentiation than populations that shared fewer megafrugivore species. This suggests that megafrugivore-mediated seed dispersal in the past may have led to frequent gene flow among populations. In comparison, extant frugivore diversity only decreased genetic differentiation in the small-fruited palm. Furthermore, genetic differentiation of all palm species decreased with landscape connectivity (i.e. environmental suitability, forest cover and river density) and human impact (i.e. road density), while migration rates of the small-fruit palm increased with road density. Synthesis. Our results suggest that the legacy of megafrugivores regularly achieving long dispersal distances is still reflected in the population genetics of palms that were formerly dispersed by such animals. Furthermore, low genetic differentiation was possibly maintained after the megafauna extinctions through alternative dispersal (e.g. human- or river-mediated), long generation times and long lifespans of these megafruit palms. Our study illustrates how species interactions that happened >1000 years ago can leave imprints in their population genetics.

KW - Arecaceae

KW - ddRAD

KW - genetic differentiation

KW - megafauna extinction

KW - population genomics

KW - recent migration rate

KW - seed dispersal

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DO - 10.1111/1365-2745.14340

M3 - Journal article

AN - SCOPUS:85194828347

SN - 0022-0477

VL - 112

SP - 1583

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JO - Journal of Ecology

JF - Journal of Ecology

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ER -

Genomic signatures of past megafrugivore-mediated dispersal in Malagasy palms

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