Genetic variation in reproductive timing in a long-lived herbaceous perennial

Will J. Reed; Jennifer L. Ison; Amy Waananen; Frank H. Shaw; Stuart Wagenius; Ruth G. Shaw

doi:10.1002/ajb2.16072

Genetic variation in reproductive timing in a long-lived herbaceous perennial

Will J. Reed, Jennifer L. Ison, Amy Waananen, Frank H. Shaw, Stuart Wagenius, Ruth G. Shaw

Ecology, Evolution and Behavior

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

Premise: Reproductive fitness of individual plants depends on the timing of flowering, especially in mate-limited populations, such as those in fragmented habitats. When flowering time traits are associated with differential reproductive success, the narrow-sense heritability (h²) of traits will determine how rapidly trait means evolve in response to selection. Heritability of flowering time is documented in many annual plants. However, estimating h² of flowering time in perennials presents additional methodological challenges, often including paternity assignment and trait expression over multiple years. Methods: We evaluated the h² of onset and duration of flowering using offspring–midparent regressions and restricted maximum likelihood methods in an experimental population of an iterocarpic, perennial, herbaceous plant, Echinacea angustifolia, growing in natural conditions. We assessed the flowering time of the parental cohort in 2005 and 2006; the offspring in 2014 through 2017. We also examined the effects of the paternity assignment from Cervus and MasterBayes on estimates of h². Results: We found substantial h² for onset and duration of flowering. We also observed variation in estimates among years. The most reliable estimates for both traits fell in the range of 0.1–0.17. We found evidence of a genotype by year interaction for onset of flowering and strong evidence that genotypes are consistent in their duration of flowering across years. Conclusions: Substantial heritabilities in this population imply the capacity for a response to natural selection, while also suggesting the potential for differential contributions to adaptive evolution among seasons.

Original language	English (US)
Pages (from-to)	1861-1874
Number of pages	14
Journal	American journal of botany
Volume	109
Issue number	11
DOIs	https://doi.org/10.1002/ajb2.16072
State	Published - Nov 2022

Bibliographical note

Funding Information:
The authors thank Gretel Kiefer for supervising data collection in the field and managing the phenology database. We thank the many interns and field assistants who gathered data and maintained experimental plots. We also thank A. Bewley, M. M. N. Incarnato, R. Johnson, J. Klamfoth, L. Leventhal, A. Pearson, D. Reitz, and M. Stevens for genotyping assistance. We are grateful for S. Mazer's valuable feedback on an early version of this manuscript. We gratefully acknowledge support from the U.S. National Science Foundation (Awards 0083468, 0521245, 0544970, 0545072, 1051791, 1052165, 1125997, 1355187, 1555997 and 1557075, including REU, ROA, RET & RAHSS supplements). The Wagenius family and the Minnesota Department of Natural Resources graciously provided land for experimental plots and facilitated their establishment and management. We thank the anonymous reviewers of this manuscript for providing thoughtful and helpful comments that improved this article.

Funding Information:
The authors thank Gretel Kiefer for supervising data collection in the field and managing the phenology database. We thank the many interns and field assistants who gathered data and maintained experimental plots. We also thank A. Bewley, M. M. N. Incarnato, R. Johnson, J. Klamfoth, L. Leventhal, A. Pearson, D. Reitz, and M. Stevens for genotyping assistance. We are grateful for S. Mazer's valuable feedback on an early version of this manuscript. We gratefully acknowledge support from the U.S. National Science Foundation (Awards 0083468, 0521245, 0544970, 0545072, 1051791, 1052165, 1125997, 1355187, 1555997 and 1557075, including REU, ROA, RET & RAHSS supplements). The Wagenius family and the Minnesota Department of Natural Resources graciously provided land for experimental plots and facilitated their establishment and management. We thank the anonymous reviewers of this manuscript for providing thoughtful and helpful comments that improved this article.

Publisher Copyright:
© 2022 Botanical Society of America.

Keywords

assortative mating
Asteraceae
Echinacea angustifolia
flowering phenology
heritability
offspring–midparent regression
paternity analysis
restricted maximum likelihood

PubMed: MeSH publication types

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

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10.1002/ajb2.16072

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@article{5fb39626556f4a94a843c9f2fe6f5594,

title = "Genetic variation in reproductive timing in a long-lived herbaceous perennial",

abstract = "Premise: Reproductive fitness of individual plants depends on the timing of flowering, especially in mate-limited populations, such as those in fragmented habitats. When flowering time traits are associated with differential reproductive success, the narrow-sense heritability (h2) of traits will determine how rapidly trait means evolve in response to selection. Heritability of flowering time is documented in many annual plants. However, estimating h2 of flowering time in perennials presents additional methodological challenges, often including paternity assignment and trait expression over multiple years. Methods: We evaluated the h2 of onset and duration of flowering using offspring–midparent regressions and restricted maximum likelihood methods in an experimental population of an iterocarpic, perennial, herbaceous plant, Echinacea angustifolia, growing in natural conditions. We assessed the flowering time of the parental cohort in 2005 and 2006; the offspring in 2014 through 2017. We also examined the effects of the paternity assignment from Cervus and MasterBayes on estimates of h2. Results: We found substantial h2 for onset and duration of flowering. We also observed variation in estimates among years. The most reliable estimates for both traits fell in the range of 0.1–0.17. We found evidence of a genotype by year interaction for onset of flowering and strong evidence that genotypes are consistent in their duration of flowering across years. Conclusions: Substantial heritabilities in this population imply the capacity for a response to natural selection, while also suggesting the potential for differential contributions to adaptive evolution among seasons.",

keywords = "assortative mating, Asteraceae, Echinacea angustifolia, flowering phenology, heritability, offspring–midparent regression, paternity analysis, restricted maximum likelihood",

author = "Reed, {Will J.} and Ison, {Jennifer L.} and Amy Waananen and Shaw, {Frank H.} and Stuart Wagenius and Shaw, {Ruth G.}",

note = "Funding Information: The authors thank Gretel Kiefer for supervising data collection in the field and managing the phenology database. We thank the many interns and field assistants who gathered data and maintained experimental plots. We also thank A. Bewley, M. M. N. Incarnato, R. Johnson, J. Klamfoth, L. Leventhal, A. Pearson, D. Reitz, and M. Stevens for genotyping assistance. We are grateful for S. Mazer's valuable feedback on an early version of this manuscript. We gratefully acknowledge support from the U.S. National Science Foundation (Awards 0083468, 0521245, 0544970, 0545072, 1051791, 1052165, 1125997, 1355187, 1555997 and 1557075, including REU, ROA, RET & RAHSS supplements). The Wagenius family and the Minnesota Department of Natural Resources graciously provided land for experimental plots and facilitated their establishment and management. We thank the anonymous reviewers of this manuscript for providing thoughtful and helpful comments that improved this article. Funding Information: The authors thank Gretel Kiefer for supervising data collection in the field and managing the phenology database. We thank the many interns and field assistants who gathered data and maintained experimental plots. We also thank A. Bewley, M. M. N. Incarnato, R. Johnson, J. Klamfoth, L. Leventhal, A. Pearson, D. Reitz, and M. Stevens for genotyping assistance. We are grateful for S. Mazer's valuable feedback on an early version of this manuscript. We gratefully acknowledge support from the U.S. National Science Foundation (Awards 0083468, 0521245, 0544970, 0545072, 1051791, 1052165, 1125997, 1355187, 1555997 and 1557075, including REU, ROA, RET & RAHSS supplements). The Wagenius family and the Minnesota Department of Natural Resources graciously provided land for experimental plots and facilitated their establishment and management. We thank the anonymous reviewers of this manuscript for providing thoughtful and helpful comments that improved this article. Publisher Copyright: {\textcopyright} 2022 Botanical Society of America.",

year = "2022",

month = nov,

doi = "10.1002/ajb2.16072",

language = "English (US)",

volume = "109",

pages = "1861--1874",

journal = "American journal of botany",

issn = "0002-9122",

publisher = "John Wiley & Sons Inc.",

number = "11",

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TY - JOUR

T1 - Genetic variation in reproductive timing in a long-lived herbaceous perennial

AU - Reed, Will J.

AU - Ison, Jennifer L.

AU - Waananen, Amy

AU - Shaw, Frank H.

AU - Wagenius, Stuart

AU - Shaw, Ruth G.

N1 - Funding Information: The authors thank Gretel Kiefer for supervising data collection in the field and managing the phenology database. We thank the many interns and field assistants who gathered data and maintained experimental plots. We also thank A. Bewley, M. M. N. Incarnato, R. Johnson, J. Klamfoth, L. Leventhal, A. Pearson, D. Reitz, and M. Stevens for genotyping assistance. We are grateful for S. Mazer's valuable feedback on an early version of this manuscript. We gratefully acknowledge support from the U.S. National Science Foundation (Awards 0083468, 0521245, 0544970, 0545072, 1051791, 1052165, 1125997, 1355187, 1555997 and 1557075, including REU, ROA, RET & RAHSS supplements). The Wagenius family and the Minnesota Department of Natural Resources graciously provided land for experimental plots and facilitated their establishment and management. We thank the anonymous reviewers of this manuscript for providing thoughtful and helpful comments that improved this article. Funding Information: The authors thank Gretel Kiefer for supervising data collection in the field and managing the phenology database. We thank the many interns and field assistants who gathered data and maintained experimental plots. We also thank A. Bewley, M. M. N. Incarnato, R. Johnson, J. Klamfoth, L. Leventhal, A. Pearson, D. Reitz, and M. Stevens for genotyping assistance. We are grateful for S. Mazer's valuable feedback on an early version of this manuscript. We gratefully acknowledge support from the U.S. National Science Foundation (Awards 0083468, 0521245, 0544970, 0545072, 1051791, 1052165, 1125997, 1355187, 1555997 and 1557075, including REU, ROA, RET & RAHSS supplements). The Wagenius family and the Minnesota Department of Natural Resources graciously provided land for experimental plots and facilitated their establishment and management. We thank the anonymous reviewers of this manuscript for providing thoughtful and helpful comments that improved this article. Publisher Copyright: © 2022 Botanical Society of America.

PY - 2022/11

Y1 - 2022/11

N2 - Premise: Reproductive fitness of individual plants depends on the timing of flowering, especially in mate-limited populations, such as those in fragmented habitats. When flowering time traits are associated with differential reproductive success, the narrow-sense heritability (h2) of traits will determine how rapidly trait means evolve in response to selection. Heritability of flowering time is documented in many annual plants. However, estimating h2 of flowering time in perennials presents additional methodological challenges, often including paternity assignment and trait expression over multiple years. Methods: We evaluated the h2 of onset and duration of flowering using offspring–midparent regressions and restricted maximum likelihood methods in an experimental population of an iterocarpic, perennial, herbaceous plant, Echinacea angustifolia, growing in natural conditions. We assessed the flowering time of the parental cohort in 2005 and 2006; the offspring in 2014 through 2017. We also examined the effects of the paternity assignment from Cervus and MasterBayes on estimates of h2. Results: We found substantial h2 for onset and duration of flowering. We also observed variation in estimates among years. The most reliable estimates for both traits fell in the range of 0.1–0.17. We found evidence of a genotype by year interaction for onset of flowering and strong evidence that genotypes are consistent in their duration of flowering across years. Conclusions: Substantial heritabilities in this population imply the capacity for a response to natural selection, while also suggesting the potential for differential contributions to adaptive evolution among seasons.

AB - Premise: Reproductive fitness of individual plants depends on the timing of flowering, especially in mate-limited populations, such as those in fragmented habitats. When flowering time traits are associated with differential reproductive success, the narrow-sense heritability (h2) of traits will determine how rapidly trait means evolve in response to selection. Heritability of flowering time is documented in many annual plants. However, estimating h2 of flowering time in perennials presents additional methodological challenges, often including paternity assignment and trait expression over multiple years. Methods: We evaluated the h2 of onset and duration of flowering using offspring–midparent regressions and restricted maximum likelihood methods in an experimental population of an iterocarpic, perennial, herbaceous plant, Echinacea angustifolia, growing in natural conditions. We assessed the flowering time of the parental cohort in 2005 and 2006; the offspring in 2014 through 2017. We also examined the effects of the paternity assignment from Cervus and MasterBayes on estimates of h2. Results: We found substantial h2 for onset and duration of flowering. We also observed variation in estimates among years. The most reliable estimates for both traits fell in the range of 0.1–0.17. We found evidence of a genotype by year interaction for onset of flowering and strong evidence that genotypes are consistent in their duration of flowering across years. Conclusions: Substantial heritabilities in this population imply the capacity for a response to natural selection, while also suggesting the potential for differential contributions to adaptive evolution among seasons.

KW - assortative mating

KW - Asteraceae

KW - Echinacea angustifolia

KW - flowering phenology

KW - heritability

KW - offspring–midparent regression

KW - paternity analysis

KW - restricted maximum likelihood

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JO - American journal of botany

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ER -

Genetic variation in reproductive timing in a long-lived herbaceous perennial

Abstract

Bibliographical note

Keywords

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