Inferring dispersal across a fragmented landscape using reconstructed families in the Glanville fritillary butterfly

Toby Fountain, Arild Husby, Etsuko Nonaka, Michelle DiLeo, Janne H. Korhonen, Pasi Rastas, Torsti Michael Schulz, Marjo Anna Kaarina Saastamoinen, Ilkka Aulis Hanski

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Dispersal is important for determining both species ecological processes, such as population viability, and its evolutionary processes, like gene flow and local adaptation. Yet obtaining accurate estimates in the wild through direct observation can be challenging or even impossible, particularly over large spatial and temporal scales. Genotyping many individuals from wild populations can provide detailed inferences about dispersal. We therefore utilized genomewide marker data to estimate dispersal in the classic metapopulation of the Glanville fritillary butterfly (Melitaea cinxia L.), in the Aland Islands in SW Finland. This is an ideal system to test the effectiveness of this approach due to the wealth of information already available covering dispersal across small spatial and temporal scales, but lack of information at larger spatial and temporal scales. We sampled three larvae per larval family group from 3732 groups over a six-year period and genotyped for 272 SNPs across the genome. We used this empirical data set to reconstruct cases where full-sibs were detected in different local populations to infer female effective dispersal distance, that is, dispersal events directly contributing to gene flow. On average this was one kilometre, closely matching previous dispersal estimates made using direct observation. To evaluate our power to detect full-sib families, we performed forward simulations using an individual-based model constructed and parameterized for the Glanville fritillary metapopulation. Using these simulations, 100% of predicted full-sibs were correct and over 98% of all true full-sib pairs were detected. We therefore demonstrate that even in a highly dynamic system with a relatively small number of markers, we can accurately reconstruct full-sib families and for the first time make inferences on female effective dispersal. This highlights the utility of this approach in systems where it has previously been impossible to obtain accurate estimates of dispersal over both ecological and evolutionary scales.

Original languageEnglish
JournalEvolutionary Applications
Volume11
Issue number3
Pages (from-to)287-297
Number of pages11
ISSN1752-4571
DOIs
Publication statusPublished - Mar 2018
MoE publication typeA1 Journal article-refereed

Fields of Science

  • 1181 Ecology, evolutionary biology
  • Colonization
  • COLONY
  • conservation genetics
  • dispersal
  • Melitaea cinxia
  • sibship reconstruction
  • SPATIAL GENETIC-STRUCTURE
  • MULTILOCUS GENOTYPE DATA
  • EXTRA-PAIR PATERNITY
  • SIBSHIP RECONSTRUCTION
  • NATURAL-POPULATIONS
  • MELITAEA-CINXIA
  • HABITAT FRAGMENTATION
  • PARENTAGE ASSIGNMENT
  • METAPOPULATION
  • MIGRATION

Cite this

@article{99b1ad226fcb4165b68e7f912f81ccd2,
title = "Inferring dispersal across a fragmented landscape using reconstructed families in the Glanville fritillary butterfly",
abstract = "Dispersal is important for determining both species ecological processes, such as population viability, and its evolutionary processes, like gene flow and local adaptation. Yet obtaining accurate estimates in the wild through direct observation can be challenging or even impossible, particularly over large spatial and temporal scales. Genotyping many individuals from wild populations can provide detailed inferences about dispersal. We therefore utilized genomewide marker data to estimate dispersal in the classic metapopulation of the Glanville fritillary butterfly (Melitaea cinxia L.), in the Aland Islands in SW Finland. This is an ideal system to test the effectiveness of this approach due to the wealth of information already available covering dispersal across small spatial and temporal scales, but lack of information at larger spatial and temporal scales. We sampled three larvae per larval family group from 3732 groups over a six-year period and genotyped for 272 SNPs across the genome. We used this empirical data set to reconstruct cases where full-sibs were detected in different local populations to infer female effective dispersal distance, that is, dispersal events directly contributing to gene flow. On average this was one kilometre, closely matching previous dispersal estimates made using direct observation. To evaluate our power to detect full-sib families, we performed forward simulations using an individual-based model constructed and parameterized for the Glanville fritillary metapopulation. Using these simulations, 100{\%} of predicted full-sibs were correct and over 98{\%} of all true full-sib pairs were detected. We therefore demonstrate that even in a highly dynamic system with a relatively small number of markers, we can accurately reconstruct full-sib families and for the first time make inferences on female effective dispersal. This highlights the utility of this approach in systems where it has previously been impossible to obtain accurate estimates of dispersal over both ecological and evolutionary scales.",
keywords = "1181 Ecology, evolutionary biology, Colonization, COLONY, conservation genetics, dispersal, Melitaea cinxia, sibship reconstruction, SPATIAL GENETIC-STRUCTURE, MULTILOCUS GENOTYPE DATA, EXTRA-PAIR PATERNITY, SIBSHIP RECONSTRUCTION, NATURAL-POPULATIONS, MELITAEA-CINXIA, HABITAT FRAGMENTATION, PARENTAGE ASSIGNMENT, METAPOPULATION, MIGRATION",
author = "Toby Fountain and Arild Husby and Etsuko Nonaka and Michelle DiLeo and Korhonen, {Janne H.} and Pasi Rastas and Schulz, {Torsti Michael} and Saastamoinen, {Marjo Anna Kaarina} and Hanski, {Ilkka Aulis}",
year = "2018",
month = "3",
doi = "10.1111/eva.12552",
language = "English",
volume = "11",
pages = "287--297",
journal = "Evolutionary Applications",
issn = "1752-4571",
publisher = "Wiley",
number = "3",

}

Inferring dispersal across a fragmented landscape using reconstructed families in the Glanville fritillary butterfly. / Fountain, Toby; Husby, Arild; Nonaka, Etsuko; DiLeo, Michelle; Korhonen, Janne H.; Rastas, Pasi; Schulz, Torsti Michael; Saastamoinen, Marjo Anna Kaarina; Hanski, Ilkka Aulis.

In: Evolutionary Applications, Vol. 11, No. 3, 03.2018, p. 287-297.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Inferring dispersal across a fragmented landscape using reconstructed families in the Glanville fritillary butterfly

AU - Fountain, Toby

AU - Husby, Arild

AU - Nonaka, Etsuko

AU - DiLeo, Michelle

AU - Korhonen, Janne H.

AU - Rastas, Pasi

AU - Schulz, Torsti Michael

AU - Saastamoinen, Marjo Anna Kaarina

AU - Hanski, Ilkka Aulis

PY - 2018/3

Y1 - 2018/3

N2 - Dispersal is important for determining both species ecological processes, such as population viability, and its evolutionary processes, like gene flow and local adaptation. Yet obtaining accurate estimates in the wild through direct observation can be challenging or even impossible, particularly over large spatial and temporal scales. Genotyping many individuals from wild populations can provide detailed inferences about dispersal. We therefore utilized genomewide marker data to estimate dispersal in the classic metapopulation of the Glanville fritillary butterfly (Melitaea cinxia L.), in the Aland Islands in SW Finland. This is an ideal system to test the effectiveness of this approach due to the wealth of information already available covering dispersal across small spatial and temporal scales, but lack of information at larger spatial and temporal scales. We sampled three larvae per larval family group from 3732 groups over a six-year period and genotyped for 272 SNPs across the genome. We used this empirical data set to reconstruct cases where full-sibs were detected in different local populations to infer female effective dispersal distance, that is, dispersal events directly contributing to gene flow. On average this was one kilometre, closely matching previous dispersal estimates made using direct observation. To evaluate our power to detect full-sib families, we performed forward simulations using an individual-based model constructed and parameterized for the Glanville fritillary metapopulation. Using these simulations, 100% of predicted full-sibs were correct and over 98% of all true full-sib pairs were detected. We therefore demonstrate that even in a highly dynamic system with a relatively small number of markers, we can accurately reconstruct full-sib families and for the first time make inferences on female effective dispersal. This highlights the utility of this approach in systems where it has previously been impossible to obtain accurate estimates of dispersal over both ecological and evolutionary scales.

AB - Dispersal is important for determining both species ecological processes, such as population viability, and its evolutionary processes, like gene flow and local adaptation. Yet obtaining accurate estimates in the wild through direct observation can be challenging or even impossible, particularly over large spatial and temporal scales. Genotyping many individuals from wild populations can provide detailed inferences about dispersal. We therefore utilized genomewide marker data to estimate dispersal in the classic metapopulation of the Glanville fritillary butterfly (Melitaea cinxia L.), in the Aland Islands in SW Finland. This is an ideal system to test the effectiveness of this approach due to the wealth of information already available covering dispersal across small spatial and temporal scales, but lack of information at larger spatial and temporal scales. We sampled three larvae per larval family group from 3732 groups over a six-year period and genotyped for 272 SNPs across the genome. We used this empirical data set to reconstruct cases where full-sibs were detected in different local populations to infer female effective dispersal distance, that is, dispersal events directly contributing to gene flow. On average this was one kilometre, closely matching previous dispersal estimates made using direct observation. To evaluate our power to detect full-sib families, we performed forward simulations using an individual-based model constructed and parameterized for the Glanville fritillary metapopulation. Using these simulations, 100% of predicted full-sibs were correct and over 98% of all true full-sib pairs were detected. We therefore demonstrate that even in a highly dynamic system with a relatively small number of markers, we can accurately reconstruct full-sib families and for the first time make inferences on female effective dispersal. This highlights the utility of this approach in systems where it has previously been impossible to obtain accurate estimates of dispersal over both ecological and evolutionary scales.

KW - 1181 Ecology, evolutionary biology

KW - Colonization

KW - COLONY

KW - conservation genetics

KW - dispersal

KW - Melitaea cinxia

KW - sibship reconstruction

KW - SPATIAL GENETIC-STRUCTURE

KW - MULTILOCUS GENOTYPE DATA

KW - EXTRA-PAIR PATERNITY

KW - SIBSHIP RECONSTRUCTION

KW - NATURAL-POPULATIONS

KW - MELITAEA-CINXIA

KW - HABITAT FRAGMENTATION

KW - PARENTAGE ASSIGNMENT

KW - METAPOPULATION

KW - MIGRATION

U2 - 10.1111/eva.12552

DO - 10.1111/eva.12552

M3 - Article

VL - 11

SP - 287

EP - 297

JO - Evolutionary Applications

JF - Evolutionary Applications

SN - 1752-4571

IS - 3

ER -