Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides

José A. Ramírez-Valiente; Nicholas J. Deacon; Julie Etterson; Alyson Center; Jed P. Sparks; Kimberlee L. Sparks; Timothy Longwell; George Pilz; Jeannine Cavender-Bares

doi:10.1111/mec.14566

Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides

José A. Ramírez-Valiente, Nicholas J. Deacon, Julie Etterson, Alyson Center, Jed P. Sparks, Kimberlee L. Sparks, Timothy Longwell, George Pilz, Jeannine Cavender-Bares

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

35 Scopus citations

Abstract

The impacts of drought are expanding worldwide as a consequence of climate change. However, there is still little knowledge of how species respond to long-term selection in seasonally dry ecosystems. In this study, we used Q_ST-F_ST comparisons to investigate (i) the role of natural selection on population genetic differentiation for a set of functional traits related to drought resistance in the seasonally dry tropical oak Quercus oleoides and (ii) the influence of water availability at the site of population origin and in experimental treatments on patterns of trait divergence. We conducted a thorough phenotypic characterization of 1912 seedlings from ten populations growing in field and greenhouse common gardens under replicated watering treatments. We also genotyped 218 individuals from the same set of populations using eleven nuclear microsatellites. Q_ST distributions for leaf lamina area, specific leaf area, leaf thickness and stomatal pore index were higher than F_ST distribution. Results were consistent across growth environments. Genetic differentiation among populations for these functional traits was associated with the index of moisture at the origin of the populations. Together, our results suggest that drought is an important selective agent for Q. oleoides and that differences in length and severity of the dry season have driven the evolution of genetic differences in functional traits.

Original language	English (US)
Pages (from-to)	2176-2192
Number of pages	17
Journal	Molecular ecology
Volume	27
Issue number	9
DOIs	https://doi.org/10.1111/mec.14566
State	Published - May 2018

Bibliographical note

Funding Information:
National Science Foundation, Grant/Award Number: IOS 0843665; Severo Ochoa excellence programme

Funding Information:
The authors wish to acknowledge the lifetime career of Dr. George Pilz, his facilitation of and contribution to this research and his dedication to teaching and mentoring generations of students at the University of Zamorano, who helped maintain the common gardens in Honduras. We thank Marileth de los Angeles Briceño for seed collection in Costa Rica and for facilitating the permit process to bring acorns. Antonio González-Rodríguez and colleagues collected and transported seeds in La Vigueta Mexican population. We gratefully acknowledge Esau M. Zúniga for permit assistance, seed collection, field management, technical assistance and help with physiological measurements. We would also like to thank Rubén Ramírez, Chris Park, Beth Fallon, Steven Brewer, Xiaojing Wei, Matthew Kaproth, Sydney Schiffner Natalie McMann, Tatiana Dimugno, Nolan Radziej and all Zamorano undergraduate students who participated in field and laboratory help. We also thank the Plant Growth Facilities staff, particularly Roger Meissner and Pamela Warnke for their technical support during the development of the greenhouse experiment. The project was funded by the National Science Foundation IOS 0843665 to JC-B, JRE and JS. JAR-V was also supported by a postdoctoral fellowship from the Severo Ochoa excellence programme.

Publisher Copyright:
© 2018 John Wiley & Sons Ltd

Keywords

adaptive evolution
ecotypic divergence
local adaptation
oaks
specific leaf area

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access

10.1111/mec.14566

OpenUrl availability

Full text

Cite this

Ramírez-Valiente, J. A., Deacon, N. J., Etterson, J., Center, A., Sparks, J. P., Sparks, K. L., Longwell, T., Pilz, G., & Cavender-Bares, J. (2018). Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides. Molecular ecology, 27(9), 2176-2192. https://doi.org/10.1111/mec.14566

Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides. / Ramírez-Valiente, José A.; Deacon, Nicholas J.; Etterson, Julie et al.
In: Molecular ecology, Vol. 27, No. 9, 05.2018, p. 2176-2192.

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

Ramírez-Valiente, JA, Deacon, NJ, Etterson, J, Center, A, Sparks, JP, Sparks, KL, Longwell, T, Pilz, G & Cavender-Bares, J 2018, 'Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides', Molecular ecology, vol. 27, no. 9, pp. 2176-2192. https://doi.org/10.1111/mec.14566

@article{0ea73580ae104d179137abdcf9c9fcc2,

title = "Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides",

abstract = "The impacts of drought are expanding worldwide as a consequence of climate change. However, there is still little knowledge of how species respond to long-term selection in seasonally dry ecosystems. In this study, we used QST-FST comparisons to investigate (i) the role of natural selection on population genetic differentiation for a set of functional traits related to drought resistance in the seasonally dry tropical oak Quercus oleoides and (ii) the influence of water availability at the site of population origin and in experimental treatments on patterns of trait divergence. We conducted a thorough phenotypic characterization of 1912 seedlings from ten populations growing in field and greenhouse common gardens under replicated watering treatments. We also genotyped 218 individuals from the same set of populations using eleven nuclear microsatellites. QST distributions for leaf lamina area, specific leaf area, leaf thickness and stomatal pore index were higher than FST distribution. Results were consistent across growth environments. Genetic differentiation among populations for these functional traits was associated with the index of moisture at the origin of the populations. Together, our results suggest that drought is an important selective agent for Q. oleoides and that differences in length and severity of the dry season have driven the evolution of genetic differences in functional traits.",

keywords = "adaptive evolution, ecotypic divergence, local adaptation, oaks, specific leaf area",

author = "Ram{\'i}rez-Valiente, {Jos{\'e} A.} and Deacon, {Nicholas J.} and Julie Etterson and Alyson Center and Sparks, {Jed P.} and Sparks, {Kimberlee L.} and Timothy Longwell and George Pilz and Jeannine Cavender-Bares",

note = "Funding Information: National Science Foundation, Grant/Award Number: IOS 0843665; Severo Ochoa excellence programme Funding Information: The authors wish to acknowledge the lifetime career of Dr. George Pilz, his facilitation of and contribution to this research and his dedication to teaching and mentoring generations of students at the University of Zamorano, who helped maintain the common gardens in Honduras. We thank Marileth de los Angeles Brice{\~n}o for seed collection in Costa Rica and for facilitating the permit process to bring acorns. Antonio Gonz{\'a}lez-Rodr{\'i}guez and colleagues collected and transported seeds in La Vigueta Mexican population. We gratefully acknowledge Esau M. Z{\'u}niga for permit assistance, seed collection, field management, technical assistance and help with physiological measurements. We would also like to thank Rub{\'e}n Ram{\'i}rez, Chris Park, Beth Fallon, Steven Brewer, Xiaojing Wei, Matthew Kaproth, Sydney Schiffner Natalie McMann, Tatiana Dimugno, Nolan Radziej and all Zamorano undergraduate students who participated in field and laboratory help. We also thank the Plant Growth Facilities staff, particularly Roger Meissner and Pamela Warnke for their technical support during the development of the greenhouse experiment. The project was funded by the National Science Foundation IOS 0843665 to JC-B, JRE and JS. JAR-V was also supported by a postdoctoral fellowship from the Severo Ochoa excellence programme. Publisher Copyright: {\textcopyright} 2018 John Wiley & Sons Ltd",

year = "2018",

month = may,

doi = "10.1111/mec.14566",

language = "English (US)",

volume = "27",

pages = "2176--2192",

journal = "Molecular ecology",

issn = "0962-1083",

publisher = "Wiley-Blackwell",

number = "9",

}

TY - JOUR

T1 - Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides

AU - Ramírez-Valiente, José A.

AU - Deacon, Nicholas J.

AU - Etterson, Julie

AU - Center, Alyson

AU - Sparks, Jed P.

AU - Sparks, Kimberlee L.

AU - Longwell, Timothy

AU - Pilz, George

AU - Cavender-Bares, Jeannine

N1 - Funding Information: National Science Foundation, Grant/Award Number: IOS 0843665; Severo Ochoa excellence programme Funding Information: The authors wish to acknowledge the lifetime career of Dr. George Pilz, his facilitation of and contribution to this research and his dedication to teaching and mentoring generations of students at the University of Zamorano, who helped maintain the common gardens in Honduras. We thank Marileth de los Angeles Briceño for seed collection in Costa Rica and for facilitating the permit process to bring acorns. Antonio González-Rodríguez and colleagues collected and transported seeds in La Vigueta Mexican population. We gratefully acknowledge Esau M. Zúniga for permit assistance, seed collection, field management, technical assistance and help with physiological measurements. We would also like to thank Rubén Ramírez, Chris Park, Beth Fallon, Steven Brewer, Xiaojing Wei, Matthew Kaproth, Sydney Schiffner Natalie McMann, Tatiana Dimugno, Nolan Radziej and all Zamorano undergraduate students who participated in field and laboratory help. We also thank the Plant Growth Facilities staff, particularly Roger Meissner and Pamela Warnke for their technical support during the development of the greenhouse experiment. The project was funded by the National Science Foundation IOS 0843665 to JC-B, JRE and JS. JAR-V was also supported by a postdoctoral fellowship from the Severo Ochoa excellence programme. Publisher Copyright: © 2018 John Wiley & Sons Ltd

PY - 2018/5

Y1 - 2018/5

N2 - The impacts of drought are expanding worldwide as a consequence of climate change. However, there is still little knowledge of how species respond to long-term selection in seasonally dry ecosystems. In this study, we used QST-FST comparisons to investigate (i) the role of natural selection on population genetic differentiation for a set of functional traits related to drought resistance in the seasonally dry tropical oak Quercus oleoides and (ii) the influence of water availability at the site of population origin and in experimental treatments on patterns of trait divergence. We conducted a thorough phenotypic characterization of 1912 seedlings from ten populations growing in field and greenhouse common gardens under replicated watering treatments. We also genotyped 218 individuals from the same set of populations using eleven nuclear microsatellites. QST distributions for leaf lamina area, specific leaf area, leaf thickness and stomatal pore index were higher than FST distribution. Results were consistent across growth environments. Genetic differentiation among populations for these functional traits was associated with the index of moisture at the origin of the populations. Together, our results suggest that drought is an important selective agent for Q. oleoides and that differences in length and severity of the dry season have driven the evolution of genetic differences in functional traits.

AB - The impacts of drought are expanding worldwide as a consequence of climate change. However, there is still little knowledge of how species respond to long-term selection in seasonally dry ecosystems. In this study, we used QST-FST comparisons to investigate (i) the role of natural selection on population genetic differentiation for a set of functional traits related to drought resistance in the seasonally dry tropical oak Quercus oleoides and (ii) the influence of water availability at the site of population origin and in experimental treatments on patterns of trait divergence. We conducted a thorough phenotypic characterization of 1912 seedlings from ten populations growing in field and greenhouse common gardens under replicated watering treatments. We also genotyped 218 individuals from the same set of populations using eleven nuclear microsatellites. QST distributions for leaf lamina area, specific leaf area, leaf thickness and stomatal pore index were higher than FST distribution. Results were consistent across growth environments. Genetic differentiation among populations for these functional traits was associated with the index of moisture at the origin of the populations. Together, our results suggest that drought is an important selective agent for Q. oleoides and that differences in length and severity of the dry season have driven the evolution of genetic differences in functional traits.

KW - adaptive evolution

KW - ecotypic divergence

KW - local adaptation

KW - oaks

KW - specific leaf area

UR - http://www.scopus.com/inward/record.url?scp=85046012617&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85046012617&partnerID=8YFLogxK

U2 - 10.1111/mec.14566

DO - 10.1111/mec.14566

M3 - Article

C2 - 29577469

AN - SCOPUS:85046012617

SN - 0962-1083

VL - 27

SP - 2176

EP - 2192

JO - Molecular ecology

JF - Molecular ecology

IS - 9

ER -

Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides

Abstract

Bibliographical note

Keywords

UN SDGs

Access

OpenUrl availability

Other files and links

Fingerprint

Cite this