Using long‐term data for a reintroduced population to empirically estimate future consequences of inbreeding
Inbreeding depression is an important long‐term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting fu...
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| Published in | Conservation biology Vol. 35; no. 3; pp. 859 - 869 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Blackwell Publishing Ltd
01.06.2021
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0888-8892 1523-1739 1523-1739 |
| DOI | 10.1111/cobi.13646 |
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| Abstract | Inbreeding depression is an important long‐term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting future population consequences is especially difficult because this also requires projecting future inbreeding levels and their impacts on long‐term population dynamics, which are subject to many uncertainties. We illustrate how such projections can be derived through Bayesian state‐space modeling methods based on a 26‐year data set for North Island Robins (Petroica longipes) reintroduced to Tiritiri Matangi Island in 1992. We used pedigree data to model increases in the average inbreeding level (F) over time based on kinship of possible breeding pairs and to estimate empirically Ne/N (effective/census population size). We used multiple imputation to model the unknown components of inbreeding coefficients, which allowed us to estimate effects of inbreeding on survival for all 1458 birds in the data set while modeling density dependence and environmental stochasticity. This modeling indicated that inbreeding reduced juvenile survival (1.83 lethal equivalents [SE 0.81]) and may have reduced subsequent adult survival (0.44 lethal equivalents [0.81]) but had no apparent effect on numbers of fledglings produced. Average inbreeding level increased to 0.10 (SE 0.001) as the population grew from 33 (0.3) to 160 (6) individuals over the 25 years, giving a Ne/N ratio of 0.56 (0.01). Based on a model that also incorporated habitat regeneration, the population was projected to reach a maximum of 331–1144 birds (median 726) in 2130, then to begin a slow decline. Without inbreeding, the population would be expected stabilize at 887–1465 birds (median 1131). Such analysis, therefore, makes it possible to empirically derive the information needed for rational decisions about inbreeding management while accounting for multiple sources of uncertainty.
Uso de Datos a Largo Plazo de una Población Reintroducida para Estimar Empíricamente las Consecuencias Futuras de la Endogamia
Resumen
La depresión endogámica es una amenaza importante a largo plazo para las poblaciones reintroducidas. Sin embargo, es complicado estimar la fuerza de la depresión endogámica en las poblaciones silvestres porque los datos sobre el linaje sin duda estarán incompletos y porque se necesitan datos sólidos sobre la supervivencia y la reproducción. Es especialmente difícil predecir las consecuencias poblacionales a futuro pues esto requiere proyectar a futuro los niveles de endogamia y sus impactos sobre las dinámicas poblacionales a largo plazo, las cuales están sujetas a muchas incertidumbres. Ilustramos cómo dichas proyecciones pueden derivarse mediante métodos de modelado bayesiano de estado‐espacio basados en un conjunto de datos obtenidos durante 26 años para los tordos de la Isla del Norte (Petroica longipes) reintroducidos a la isla Tiritiri Matangi en 1992. Usamos datos de linaje para modelar los incrementos en el nivel promedio de endogamia (F̲) a lo largo del tiempo con base en el parentesco de las posibles parejas reproductoras y para estimar empíricamente Ne/N (tamaño poblacional efectivo/por censo). Usamos una imputación múltiple para modelar los componentes desconocidos de los coeficientes de endogamia, lo que nos permitió estimar los efectos de la endogamia sobre la supervivencia para todas las aves (1458) incluidas en el conjunto de datos a la vez que modelamos la dependencia de la densidad y la estocasticidad ambiental. Este modelado indicó que la endogamia redujo la supervivencia juvenil (1.83 equivalentes letales [SE 0.81]) y podría haber reducido la subsecuente supervivencia adulta (0.44 equivalentes letales [0.81]) pero no tuvo un efecto aparente sobre los números de polluelos producidos. El nivel promedio de endogamia incrementó a 0.10 (SE 0.001) conforme la población creció de 33 (0.3) a 160 (6) individuos a lo largo de los 25 años, lo que resultó en una proporción Ne/N de 0.56 (0.01). Con base en un modelo que también incorporó la regeneración del hábitat, se proyectó que la población alcanzaría un máximo de 331–1144 aves (mediana: 726) para 2130 y después comenzaría una lenta disminución. Sin la endogamia, se esperaría que la población se estabilizaría con 887–1465 (mediana: 1131) aves. Por lo tanto, dicho análisis hace posible la derivación empírica de la información necesaria para las decisiones racionales sobre el manejo de la endogamia a la vez que considera a varias fuentes de incertidumbre.
Article Impact Statement: Empirically estimating the future consequences of inbreeding allows rational long‐term management of reintroduced populations. |
|---|---|
| AbstractList | Inbreeding depression is an important long‐term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting future population consequences is especially difficult because this also requires projecting future inbreeding levels and their impacts on long‐term population dynamics, which are subject to many uncertainties. We illustrate how such projections can be derived through Bayesian state‐space modeling methods based on a 26‐year data set for North Island Robins (
Petroica longipes
) reintroduced to Tiritiri Matangi Island in 1992. We used pedigree data to model increases in the average inbreeding level (
F
) over time based on kinship of possible breeding pairs and to estimate empirically
N
e
/N
(effective/census population size). We used multiple imputation to model the unknown components of inbreeding coefficients, which allowed us to estimate effects of inbreeding on survival for all 1458 birds in the data set while modeling density dependence and environmental stochasticity. This modeling indicated that inbreeding reduced juvenile survival (1.83 lethal equivalents [SE 0.81]) and may have reduced subsequent adult survival (0.44 lethal equivalents [0.81]) but had no apparent effect on numbers of fledglings produced. Average inbreeding level increased to 0.10 (SE 0.001) as the population grew from 33 (0.3) to 160 (6) individuals over the 25 years, giving a
ratio of 0.56 (0.01). Based on a model that also incorporated habitat regeneration, the population was projected to reach a maximum of 331–1144 birds (median 726) in 2130, then to begin a slow decline. Without inbreeding, the population would be expected stabilize at 887–1465 birds (median 1131). Such analysis, therefore, makes it possible to empirically derive the information needed for rational decisions about inbreeding management while accounting for multiple sources of uncertainty.
Article Impact Statement
: Empirically estimating the future consequences of inbreeding allows rational long‐term management of reintroduced populations. Inbreeding depression is an important long-term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting future population consequences is especially difficult because this also requires projecting future inbreeding levels and their impacts on long-term population dynamics, which are subject to many uncertainties. We illustrate how such projections can be derived through Bayesian state-space modeling methods based on a 26-year data set for North Island Robins (Petroica longipes) reintroduced to Tiritiri Matangi Island in 1992. We used pedigree data to model increases in the average inbreeding level (F) over time based on kinship of possible breeding pairs and to estimate empirically Ne /N (effective/census population size). We used multiple imputation to model the unknown components of inbreeding coefficients, which allowed us to estimate effects of inbreeding on survival for all 1458 birds in the data set while modeling density dependence and environmental stochasticity. This modeling indicated that inbreeding reduced juvenile survival (1.83 lethal equivalents [SE 0.81]) and may have reduced subsequent adult survival (0.44 lethal equivalents [0.81]) but had no apparent effect on numbers of fledglings produced. Average inbreeding level increased to 0.10 (SE 0.001) as the population grew from 33 (0.3) to 160 (6) individuals over the 25 years, giving a Ne/N ratio of 0.56 (0.01). Based on a model that also incorporated habitat regeneration, the population was projected to reach a maximum of 331-1144 birds (median 726) in 2130, then to begin a slow decline. Without inbreeding, the population would be expected stabilize at 887-1465 birds (median 1131). Such analysis, therefore, makes it possible to empirically derive the information needed for rational decisions about inbreeding management while accounting for multiple sources of uncertainty.Inbreeding depression is an important long-term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting future population consequences is especially difficult because this also requires projecting future inbreeding levels and their impacts on long-term population dynamics, which are subject to many uncertainties. We illustrate how such projections can be derived through Bayesian state-space modeling methods based on a 26-year data set for North Island Robins (Petroica longipes) reintroduced to Tiritiri Matangi Island in 1992. We used pedigree data to model increases in the average inbreeding level (F) over time based on kinship of possible breeding pairs and to estimate empirically Ne /N (effective/census population size). We used multiple imputation to model the unknown components of inbreeding coefficients, which allowed us to estimate effects of inbreeding on survival for all 1458 birds in the data set while modeling density dependence and environmental stochasticity. This modeling indicated that inbreeding reduced juvenile survival (1.83 lethal equivalents [SE 0.81]) and may have reduced subsequent adult survival (0.44 lethal equivalents [0.81]) but had no apparent effect on numbers of fledglings produced. Average inbreeding level increased to 0.10 (SE 0.001) as the population grew from 33 (0.3) to 160 (6) individuals over the 25 years, giving a Ne/N ratio of 0.56 (0.01). Based on a model that also incorporated habitat regeneration, the population was projected to reach a maximum of 331-1144 birds (median 726) in 2130, then to begin a slow decline. Without inbreeding, the population would be expected stabilize at 887-1465 birds (median 1131). Such analysis, therefore, makes it possible to empirically derive the information needed for rational decisions about inbreeding management while accounting for multiple sources of uncertainty. Inbreeding depression is an important long-term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting future population consequences is especially difficult because this also requires projecting future inbreeding levels and their impacts on long-term population dynamics, which are subject to many uncertainties. We illustrate how such projections can be derived through Bayesian state-space modeling methods based on a 26-year data set for North Island Robins (Petroica longipes) reintroduced to Tiritiri Matangi Island in 1992. We used pedigree data to model increases in the average inbreeding level (F) over time based on kinship of possible breeding pairs and to estimate empirically Ne/N (effective/census population size). We used multiple imputation to model the unknown components of inbreeding coefficients, which allowed us to estimate effects of inbreeding on survival for all 1458 birds in the data set while modeling density dependence and environmental stochasticity. This modeling indicated that inbreeding reduced juvenile survival (1.83 lethal equivalents [SE 0.81]) and may have reduced subsequent adult survival (0.44 lethal equivalents [0.81]) but had no apparent effect on numbers of fledglings produced. Average inbreeding level increased to 0.10 (SE 0.001) as the population grew from 33 (0.3) to 160 (6) individuals over the 25 years, giving a urn:x-wiley:08888892:media:cobi13646:cobi13646-math-0001 ratio of 0.56 (0.01). Based on a model that also incorporated habitat regeneration, the population was projected to reach a maximum of 331–1144 birds (median 726) in 2130, then to begin a slow decline. Without inbreeding, the population would be expected stabilize at 887–1465 birds (median 1131). Such analysis, therefore, makes it possible to empirically derive the information needed for rational decisions about inbreeding management while accounting for multiple sources of uncertainty. Inbreeding depression is an important long‐term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting future population consequences is especially difficult because this also requires projecting future inbreeding levels and their impacts on long‐term population dynamics, which are subject to many uncertainties. We illustrate how such projections can be derived through Bayesian state‐space modeling methods based on a 26‐year data set for North Island Robins (Petroica longipes) reintroduced to Tiritiri Matangi Island in 1992. We used pedigree data to model increases in the average inbreeding level (F) over time based on kinship of possible breeding pairs and to estimate empirically Nₑ/N (effective/census population size). We used multiple imputation to model the unknown components of inbreeding coefficients, which allowed us to estimate effects of inbreeding on survival for all 1458 birds in the data set while modeling density dependence and environmental stochasticity. This modeling indicated that inbreeding reduced juvenile survival (1.83 lethal equivalents [SE 0.81]) and may have reduced subsequent adult survival (0.44 lethal equivalents [0.81]) but had no apparent effect on numbers of fledglings produced. Average inbreeding level increased to 0.10 (SE 0.001) as the population grew from 33 (0.3) to 160 (6) individuals over the 25 years, giving a Ne/N ratio of 0.56 (0.01). Based on a model that also incorporated habitat regeneration, the population was projected to reach a maximum of 331–1144 birds (median 726) in 2130, then to begin a slow decline. Without inbreeding, the population would be expected stabilize at 887–1465 birds (median 1131). Such analysis, therefore, makes it possible to empirically derive the information needed for rational decisions about inbreeding management while accounting for multiple sources of uncertainty. Inbreeding depression is an important long‐term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting future population consequences is especially difficult because this also requires projecting future inbreeding levels and their impacts on long‐term population dynamics, which are subject to many uncertainties. We illustrate how such projections can be derived through Bayesian state‐space modeling methods based on a 26‐year data set for North Island Robins (Petroica longipes) reintroduced to Tiritiri Matangi Island in 1992. We used pedigree data to model increases in the average inbreeding level (F) over time based on kinship of possible breeding pairs and to estimate empirically Ne/N (effective/census population size). We used multiple imputation to model the unknown components of inbreeding coefficients, which allowed us to estimate effects of inbreeding on survival for all 1458 birds in the data set while modeling density dependence and environmental stochasticity. This modeling indicated that inbreeding reduced juvenile survival (1.83 lethal equivalents [SE 0.81]) and may have reduced subsequent adult survival (0.44 lethal equivalents [0.81]) but had no apparent effect on numbers of fledglings produced. Average inbreeding level increased to 0.10 (SE 0.001) as the population grew from 33 (0.3) to 160 (6) individuals over the 25 years, giving a Ne/N ratio of 0.56 (0.01). Based on a model that also incorporated habitat regeneration, the population was projected to reach a maximum of 331–1144 birds (median 726) in 2130, then to begin a slow decline. Without inbreeding, the population would be expected stabilize at 887–1465 birds (median 1131). Such analysis, therefore, makes it possible to empirically derive the information needed for rational decisions about inbreeding management while accounting for multiple sources of uncertainty. Uso de Datos a Largo Plazo de una Población Reintroducida para Estimar Empíricamente las Consecuencias Futuras de la Endogamia Resumen La depresión endogámica es una amenaza importante a largo plazo para las poblaciones reintroducidas. Sin embargo, es complicado estimar la fuerza de la depresión endogámica en las poblaciones silvestres porque los datos sobre el linaje sin duda estarán incompletos y porque se necesitan datos sólidos sobre la supervivencia y la reproducción. Es especialmente difícil predecir las consecuencias poblacionales a futuro pues esto requiere proyectar a futuro los niveles de endogamia y sus impactos sobre las dinámicas poblacionales a largo plazo, las cuales están sujetas a muchas incertidumbres. Ilustramos cómo dichas proyecciones pueden derivarse mediante métodos de modelado bayesiano de estado‐espacio basados en un conjunto de datos obtenidos durante 26 años para los tordos de la Isla del Norte (Petroica longipes) reintroducidos a la isla Tiritiri Matangi en 1992. Usamos datos de linaje para modelar los incrementos en el nivel promedio de endogamia (F̲) a lo largo del tiempo con base en el parentesco de las posibles parejas reproductoras y para estimar empíricamente Ne/N (tamaño poblacional efectivo/por censo). Usamos una imputación múltiple para modelar los componentes desconocidos de los coeficientes de endogamia, lo que nos permitió estimar los efectos de la endogamia sobre la supervivencia para todas las aves (1458) incluidas en el conjunto de datos a la vez que modelamos la dependencia de la densidad y la estocasticidad ambiental. Este modelado indicó que la endogamia redujo la supervivencia juvenil (1.83 equivalentes letales [SE 0.81]) y podría haber reducido la subsecuente supervivencia adulta (0.44 equivalentes letales [0.81]) pero no tuvo un efecto aparente sobre los números de polluelos producidos. El nivel promedio de endogamia incrementó a 0.10 (SE 0.001) conforme la población creció de 33 (0.3) a 160 (6) individuos a lo largo de los 25 años, lo que resultó en una proporción Ne/N de 0.56 (0.01). Con base en un modelo que también incorporó la regeneración del hábitat, se proyectó que la población alcanzaría un máximo de 331–1144 aves (mediana: 726) para 2130 y después comenzaría una lenta disminución. Sin la endogamia, se esperaría que la población se estabilizaría con 887–1465 (mediana: 1131) aves. Por lo tanto, dicho análisis hace posible la derivación empírica de la información necesaria para las decisiones racionales sobre el manejo de la endogamia a la vez que considera a varias fuentes de incertidumbre. Article Impact Statement: Empirically estimating the future consequences of inbreeding allows rational long‐term management of reintroduced populations. Inbreeding depression is an important long-term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting future population consequences is especially difficult because this also requires projecting future inbreeding levels and their impacts on long-term population dynamics, which are subject to many uncertainties. We illustrate how such projections can be derived through Bayesian state-space modeling methods based on a 26-year data set for North Island Robins (Petroica longipes) reintroduced to Tiritiri Matangi Island in 1992. We used pedigree data to model increases in the average inbreeding level (F) over time based on kinship of possible breeding pairs and to estimate empirically N /N (effective/census population size). We used multiple imputation to model the unknown components of inbreeding coefficients, which allowed us to estimate effects of inbreeding on survival for all 1458 birds in the data set while modeling density dependence and environmental stochasticity. This modeling indicated that inbreeding reduced juvenile survival (1.83 lethal equivalents [SE 0.81]) and may have reduced subsequent adult survival (0.44 lethal equivalents [0.81]) but had no apparent effect on numbers of fledglings produced. Average inbreeding level increased to 0.10 (SE 0.001) as the population grew from 33 (0.3) to 160 (6) individuals over the 25 years, giving a ratio of 0.56 (0.01). Based on a model that also incorporated habitat regeneration, the population was projected to reach a maximum of 331-1144 birds (median 726) in 2130, then to begin a slow decline. Without inbreeding, the population would be expected stabilize at 887-1465 birds (median 1131). Such analysis, therefore, makes it possible to empirically derive the information needed for rational decisions about inbreeding management while accounting for multiple sources of uncertainty. Inbreeding depression is an important long‐term threat to reintroduced populations. However, the strength of inbreeding depression is difficult to estimate in wild populations because pedigree data are inevitably incomplete and because good data are needed on survival and reproduction. Predicting future population consequences is especially difficult because this also requires projecting future inbreeding levels and their impacts on long‐term population dynamics, which are subject to many uncertainties. We illustrate how such projections can be derived through Bayesian state‐space modeling methods based on a 26‐year data set for North Island Robins (Petroica longipes) reintroduced to Tiritiri Matangi Island in 1992. We used pedigree data to model increases in the average inbreeding level (F) over time based on kinship of possible breeding pairs and to estimate empirically Ne/N (effective/census population size). We used multiple imputation to model the unknown components of inbreeding coefficients, which allowed us to estimate effects of inbreeding on survival for all 1458 birds in the data set while modeling density dependence and environmental stochasticity. This modeling indicated that inbreeding reduced juvenile survival (1.83 lethal equivalents [SE 0.81]) and may have reduced subsequent adult survival (0.44 lethal equivalents [0.81]) but had no apparent effect on numbers of fledglings produced. Average inbreeding level increased to 0.10 (SE 0.001) as the population grew from 33 (0.3) to 160 (6) individuals over the 25 years, giving a Ne/N ratio of 0.56 (0.01). Based on a model that also incorporated habitat regeneration, the population was projected to reach a maximum of 331–1144 birds (median 726) in 2130, then to begin a slow decline. Without inbreeding, the population would be expected stabilize at 887–1465 birds (median 1131). Such analysis, therefore, makes it possible to empirically derive the information needed for rational decisions about inbreeding management while accounting for multiple sources of uncertainty. |
| Author | Parlato, Elizabeth H. Kwikkel, Renske Ewen, John G. McCready, Mhairi Parker, Kevin A. Berggren, Åsa Armstrong, Doug P. Egli, Barbara Dimond, Wendy J. |
| Author_xml | – sequence: 1 givenname: Doug P. orcidid: 0000-0003-0163-3435 surname: Armstrong fullname: Armstrong, Doug P. email: d.p.armstrong@massey.ac.nz organization: Massey University – sequence: 2 givenname: Elizabeth H. orcidid: 0000-0002-0787-0485 surname: Parlato fullname: Parlato, Elizabeth H. organization: Massey University – sequence: 3 givenname: Barbara surname: Egli fullname: Egli, Barbara organization: Massey University – sequence: 4 givenname: Wendy J. surname: Dimond fullname: Dimond, Wendy J. organization: The Australian National University – sequence: 5 givenname: Renske surname: Kwikkel fullname: Kwikkel, Renske organization: Van Hall Instituut – sequence: 6 givenname: Åsa surname: Berggren fullname: Berggren, Åsa organization: Swedish University of Agricultural Sciences – sequence: 7 givenname: Mhairi surname: McCready fullname: McCready, Mhairi organization: Hihi Conservation Charitable Trust – sequence: 8 givenname: Kevin A. surname: Parker fullname: Parker, Kevin A. organization: Parker Conservation – sequence: 9 givenname: John G. surname: Ewen fullname: Ewen, John G. organization: Zoological Society of London |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32997349$$D View this record in MEDLINE/PubMed https://res.slu.se/id/publ/109466$$DView record from Swedish Publication Index |
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| CitedBy_id | crossref_primary_10_1016_j_ecolmodel_2024_110662 crossref_primary_10_1111_mec_17690 crossref_primary_10_1111_acv_13019 crossref_primary_10_1111_mec_17608 crossref_primary_10_1111_1365_2656_13592 crossref_primary_10_1111_mec_16068 crossref_primary_10_1111_cobi_13843 |
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| ContentType | Journal Article |
| Copyright | 2020 Society for Conservation Biology 2020 Society for Conservation Biology. 2021, Society for Conservation Biology |
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| Keywords | Bayesian hierarchical modeling reintroducción Toutouwai poblaciones pequeñas modelado jerárquico bayesiano New Zealand population modeling North Island robin reintroduction modelado poblacional small populations tordo de la Isla del Norte Nueva Zelanda inbreeding depression depresión endogámica |
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| SubjectTerms | adults Bayesian analysis Bayesian hierarchical modeling Bayesian theory Birds Breeding Coefficients Data data collection Datasets Density dependence depresión endogámica Ecology Ekologi Environment models Equivalence habitats Inbreeding Inbreeding depression Juveniles kinship modelado jerárquico bayesiano modelado poblacional Modelling New Zealand North Island robin Nueva Zelanda Pedigree Petroica Petroica longipes poblaciones pequeñas Population Population decline Population dynamics population modeling Population number population size Populations Probability theory Regeneration Regeneration (biological) reintroducción reintroduction small populations Stochasticity Survival tordo de la Isla del Norte Toutouwai Uncertainty wildlife management |
| Title | Using long‐term data for a reintroduced population to empirically estimate future consequences of inbreeding |
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