Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations

Schrieber K, Wolf S, Wypior C, Hoehlig D, Keller SR, Hensen I, Lachmuth S (2019)
Ecology and Evolution 9(6): 3564-3576.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Schrieber, KarinUniBi; Wolf, Sabrina; Wypior, Catherina; Hoehlig, Diana; Keller, Stephen R.; Hensen, Isabell; Lachmuth, Susanne
Abstract / Bemerkung
Inbreeding and enemy infestation are common in plants and can synergistically reduce their performance. This inbreeding xenvironment (I x E) interaction may be of particular importance for the success of plant invasions if introduced populations experience a release from attack by natural enemies relative to their native conspecifics. Here, we investigate whether inbreeding affects plant infestation damage, whether inbreeding depression in growth and reproduction is mitigated by enemy release, and whether this effect is more pronounced in invasive than native plant populations. We used the invader Silene latifolia and its natural enemies as a study system. We performed two generations of experimental out- and inbreeding within eight native (European) and eight invasive (North American) populations under controlled conditions using field-collected seeds. Subsequently, we exposed the offspring to an enemy exclusion and inclusion treatment in a common garden in the species' native range to assess the interactive effects of population origin (range), breeding treatment, and enemy treatment on infestation damage, growth, and reproduction. Inbreeding increased flower and leaf infestation damage in plants from both ranges, but had opposing effects on fruit damage in native versus invasive plants. Inbreeding significantly reduced plant fitness; whereby, inbreeding depression in fruit number was higher in enemy inclusions than exclusions. This effect was equally pronounced in populations from both distribution ranges. Moreover, the magnitude of inbreeding depression in fruit number was lower in invasive than native populations. These results support that inbreeding has the potential to reduce plant defenses in S. latifolia, which magnifies inbreeding depression in the presence of enemies. However, future studies are necessary to further explore whether enemy release in the invaded habitat has actually decreased inbreeding depression and thus facilitated the persistence of inbred founder populations and invasion success.
Stichworte
biological invasion; plant defense; evolution; genetic paradox; herbivory; inbreeding; purging; Silene latifolia
Erscheinungsjahr
2019
Zeitschriftentitel
Ecology and Evolution
Band
9
Ausgabe
6
Seite(n)
3564-3576
ISSN
2045-7758
eISSN
2045-7758
Finanzierungs-Informationen
Open-Access-Publikationskosten wurden durch die Universität Bielefeld im Rahmen des DEAL-Vertrags gefördert.
Page URI
https://pub.uni-bielefeld.de/record/2935007

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Schrieber K, Wolf S, Wypior C, et al. Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations. Ecology and Evolution. 2019;9(6):3564-3576.
Schrieber, K., Wolf, S., Wypior, C., Hoehlig, D., Keller, S. R., Hensen, I., & Lachmuth, S. (2019). Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations. Ecology and Evolution, 9(6), 3564-3576. doi:10.1002/ece3.4990
Schrieber, Karin, Wolf, Sabrina, Wypior, Catherina, Hoehlig, Diana, Keller, Stephen R., Hensen, Isabell, and Lachmuth, Susanne. 2019. “Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations”. Ecology and Evolution 9 (6): 3564-3576.
Schrieber, K., Wolf, S., Wypior, C., Hoehlig, D., Keller, S. R., Hensen, I., and Lachmuth, S. (2019). Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations. Ecology and Evolution 9, 3564-3576.
Schrieber, K., et al., 2019. Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations. Ecology and Evolution, 9(6), p 3564-3576.
K. Schrieber, et al., “Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations”, Ecology and Evolution, vol. 9, 2019, pp. 3564-3576.
Schrieber, K., Wolf, S., Wypior, C., Hoehlig, D., Keller, S.R., Hensen, I., Lachmuth, S.: Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations. Ecology and Evolution. 9, 3564-3576 (2019).
Schrieber, Karin, Wolf, Sabrina, Wypior, Catherina, Hoehlig, Diana, Keller, Stephen R., Hensen, Isabell, and Lachmuth, Susanne. “Release from natural enemies mitigates inbreeding depression in native and invasive Silene latifolia populations”. Ecology and Evolution 9.6 (2019): 3564-3576.
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79 References

Daten bereitgestellt von Europe PubMed Central.

Enhanced fitness due to higher fecundity, increased defence against a specialist and tolerance towards a generalist herbivore in an invasive annual plant
AUTHOR UNKNOWN, 2009
Evolution of plant growth and defense in a continental introduction.
Agrawal AA, Hastings AP, Bradburd GS, Woods EC, Zust T, Harvey JA, Bukovinszky T., Am. Nat. 186(1), 2015
PMID: 26098351
Beyond EICA: Understanding post‐establishment evolution requires a broader evaluation of potential selection pressures
AUTHOR UNKNOWN, 2011
Effects of colonization processes on genetic diversity: differences between annual plants and tree species.
Austerlitz F, Mariette S, Machon N, Gouyon PH, Godelle B., Genetics 154(3), 2000
PMID: 10757772
lme4: Linear mixed‐effects models using Eigen and S4
AUTHOR UNKNOWN, 2014
The effect of inbreeding on defence against multiple enemies in Datura stramonium.
Bello-Bedoy R, Nunez-Farfan J., J. Evol. Biol. 24(3), 2010
PMID: 21159000
A phylogenetically controlled analysis of the roles of reproductive traits in plant invasions.
Burns JH, Ashman TL, Steets JA, Harmon-Threatt A, Knight TM., Oecologia 166(4), 2011
PMID: 21328010
Plant mating systems affect adaptive plasticity in response to herbivory.
Campbell SA, Halitschke R, Thaler JS, Kessler A., Plant J. 78(3), 2014
PMID: 24580720
Plant chemistry underlies herbivore-mediated inbreeding depression in nature.
Campbell SA, Thaler JS, Kessler A., Ecol. Lett. 16(2), 2012
PMID: 23216879
Interactions between insect herbivores and plant mating systems.
Carr DE, Eubanks MD., Annu. Rev. Entomol. 59(), 2013
PMID: 24160428
Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework
AUTHOR UNKNOWN, 2009
The genetics of inbreeding depression
AUTHOR UNKNOWN, 2009
Invasions and extinctions through the looking glass of evolutionary ecology.
Colautti RI, Alexander JM, Dlugosch KM, Keller SR, Sultan SE., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 372(1712), 2017
PMID: 27920376
Rapid adaptation to climate facilitates range expansion of an invasive plant.
Colautti RI, Barrett SC., Science 342(6156), 2013
PMID: 24136968
Is invasion success explained by the enemy release hypothesis?
AUTHOR UNKNOWN, 2004
Perspective: purging the genetic load: a review of the experimental evidence.
Crnokrak P, Barrett SC., Evolution 56(12), 2002
PMID: 12583575
Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses.
Dotterl S, Jurgens A, Seifert K, Laube T, Weissbecker B, Schutz S., New Phytol. 169(4), 2006
PMID: 16441752
Is there a genetic paradox of biological invasion?
AUTHOR UNKNOWN, 2016
Inbreeding depression is purged in the invasive insect Harmonia axyridis.
Facon B, Hufbauer RA, Tayeh A, Loiseau A, Lombaert E, Vitalis R, Guillemaud T, Lundgren JG, Estoup A., Curr. Biol. 21(5), 2011
PMID: 21333536
Role of propagule pressure in colonization success: disentangling the relative importance of demographic, genetic and habitat effects.
Hufbauer RA, Rutschmann A, Serrate B, Vermeil de Conchard H, Facon B., J. Evol. Biol. 26(8), 2013
PMID: 23724778
Evolutionary interactions between plant reproduction and defense against herbivores
AUTHOR UNKNOWN, 2015
The enemy release and EICA hypothesis revisited: Incorporating the fundamental difference between specialist and generalist herbivores
AUTHOR UNKNOWN, 2005
Constitutive and herbivore-induced structural defenses are compromised by inbreeding in Solanum carolinense (Solanaceae)
Kariyat RR, Balogh CM, Moraski RP, De Moraes CM, Mescher MC, Stephenson AG., Am. J. Bot. 100(6), 2013
PMID: IND601149106
Inbreeding in horsenettle (Solanum carolinense) alters night-time volatile emissions that guide oviposition by Manduca sexta moths.
Kariyat RR, Mauck KE, Balogh CM, Stephenson AG, Mescher MC, De Moraes CM., Proc. Biol. Sci. 280(1757), 2013
PMID: 23446531
Inbreeding alters volatile signalling phenotypes and influences tri-trophic interactions in horsenettle (Solanum carolinense L.).
Kariyat RR, Mauck KE, De Moraes CM, Stephenson AG, Mescher MC., Ecol. Lett. 15(4), 2012
PMID: 22257268
Inbreeding, herbivory, and the transcriptome of Solanum carolinense
AUTHOR UNKNOWN, 2012
Inbreeding effects in wild populations
AUTHOR UNKNOWN, 2002
Adaptation and colonization history affect the evolution of clines in two introduced species.
Keller SR, Sowell DR, Neiman M, Wolfe LM, Taylor DR., New Phytol. 183(3), 2009
PMID: 19538550

AUTHOR UNKNOWN, 2015
Research on inbreeding in the 'omic' era.
Kristensen TN, Pedersen KS, Vermeulen CJ, Loeschcke V., Trends Ecol. Evol. (Amst.) 25(1), 2009
PMID: 19733933
Habitat fragmentation, climate change, and inbreeding in plants.
Leimu R, Vergeer P, Angeloni F, Ouborg NJ., Ann. N. Y. Acad. Sci. 1195(), 2010
PMID: 20536818
Least‐Squares Means: The R package lsmeans
AUTHOR UNKNOWN, 2016
Inbreeding–environment interactions increase extinction risk
AUTHOR UNKNOWN, 2009
The relative contributions of seed and pollen movement to the local genetic structure of Silene alba
AUTHOR UNKNOWN, 1997
Local founding events as determinants of genetic structure in a plant metapopulation
AUTHOR UNKNOWN, 1995
Controls on pathogen species richness in plants' introduced and native ranges: roles of residence time, range size and host traits.
Mitchell CE, Blumenthal D, Jarosik V, Puckett EE, Pysek P., Ecol. Lett. 13(12), 2010
PMID: 20973907
Release of invasive plants from fungal and viral pathogens.
Mitchell CE, Power AG., Nature 421(6923), 2003
PMID: 12571594
The role of inbreeding and outbreeding in herbivore resistance and tolerance in Vincetoxicum hirundinaria.
Muola A, Mutikainen P, Laukkanen L, Lilley M, Leimu R., Ann. Bot. 108(3), 2011
PMID: 21803741
Demography as the basis for understanding and predicting range dynamics
AUTHOR UNKNOWN, 2014
Fitness and its role in evolutionary genetics.
Orr HA., Nat. Rev. Genet. 10(8), 2009
PMID: 19546856
Life-history evolution in range-shifting populations.
Phillips BL, Brown GP, Shine R., Ecology 91(6), 2010
PMID: 20583704
Inbreeding compromises host plant defense gene expression and improves herbivore survival.
Portman SL, Kariyat RR, Johnston MA, Stephenson AG, Marden JH., Plant Signal Behav 10(5), 2015
PMID: 26039489
R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing
AUTHOR UNKNOWN, 2017
Inbreeding-stress interactions: evolutionary and conservation consequences.
Reed DH, Fox CW, Enders LS, Kristensen TN., Ann. N. Y. Acad. Sci. 1256(), 2012
PMID: 22583046
How important is intraspecific genetic admixture to the success of colonising populations?
Rius M, Darling JA., Trends Ecol. Evol. (Amst.) 29(4), 2014
PMID: 24636862
Inbreeding depression across a nutritional stress continuum.
Schou MF, Loeschcke V, Kristensen TN., Heredity (Edinb) 115(1), 2015
PMID: 26059969
Inbreeding diminishes herbivore‐induced metabolic responses in native and invasive plant populations
AUTHOR UNKNOWN, 2018
Adaptive and non‐adaptive evolution of trait means and genetic trait correlations for herbivory resistance and performance in an invasive plant
AUTHOR UNKNOWN, 2017
Native insect herbivory overwhelms context dependence to limit complex invasion dynamics of exotic weeds.
Schultz EL, Eckberg JO, Berg SS, Louda SM, Miller TEX., Ecol. Lett. 20(11), 2017
PMID: 28901044
Interrelationships among inbreeding, herbivory, and disease on reproduction in a wild gourd
Stephenson AG, Bradley Leyshon , C. Nelson Hayes , James A. Winsor , Steven E. Travers ., Ecology 85(11), 2004
PMID: IND43714863

AUTHOR UNKNOWN, 2000
Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia
AUTHOR UNKNOWN, 2004
Increased competitive ability and herbivory tolerance in the invasive plant Sapium sebiferum
Zou Jianwen, Rogers WilliamE, Siemann Evan., Biol. Invasions 10(3), 2008
PMID: IND44015653

AUTHOR UNKNOWN, 2009
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