Can heterosis and inbreeding depression explain the maintenance of outcrossing in a cleistogamous perennial?

Acanthaceae Ruellia humilis chasmogamous cleistogamy heterosis inbreeding depression mating-system evolution mixed mating outbreeding depression selfing

Journal

American journal of botany
ISSN: 1537-2197
Titre abrégé: Am J Bot
Pays: United States
ID NLM: 0370467

Informations de publication

Date de publication:
10 2023
Historique:
revised: 17 08 2023
received: 09 06 2023
accepted: 18 08 2023
medline: 27 10 2023
pubmed: 6 9 2023
entrez: 6 9 2023
Statut: ppublish

Résumé

What maintains mixed mating is an evolutionary enigma. Cleistogamy-the production of both potentially outcrossing chasmogamous and obligately selfing cleistogamous flowers on the same individual plant-is an excellent system to study the costs of selfing. Inbreeding depression can prevent the evolution of greater selfing within populations, and heterosis in crosses between populations may further tip the balance in favor of outcrossing. Few empirical estimates of inbreeding depression and heterosis in the same system exist for cleistogamous species. We investigate the potential costs of selfing by quantifying inbreeding depression and heterosis in three populations of the cleistogamous perennial Ruellia humilis Nutt (Acanthaceae). We performed three types of hand-pollinations-self, outcross-within, and outcross-between populations-and measured seed number, germination, total flower production, and estimated cumulative fitness for the resulting progeny in a greenhouse experiment. We found moderate inbreeding depression for cumulative fitness (<30%) in two populations, but outbreeding depression for crosses within a third population (-26%). For between-population crosses, there was weak to modest heterosis (11-47%) in two of the population combinations, but modest to strong outbreeding depression (-21 to -71%) in the other four combinations. Neither inbreeding depression nor heterosis was of sufficient magnitude to explain the continued production of chasmogamous flowers given the relative energetic advantage of cleistogamous flowers previously estimated for these populations. Outbreeding depression either within or between populations makes the maintenance of chasmogamous flowers even harder to explain. More information is needed on the genetic basis of cleistogamy to resolve this conundrum. Lo que mantiene los sistemas de apareamiento mixto aún es un enigma. La cleistogamia, la producción de flores con potencial de cruzamiento casmógamas, y de flores cleistógamas obligadamente autofecundadas en la misma planta, es un excelente sistema para estudiar los costos de la autofecundación. La depresión endogámica puede prevenir la evolución hacia una mayor autofecundación dentro de las poblaciones, y la heterosis de los cruces entre poblaciones puede inclinar aún más la balanza a favor del cruzamiento. Existen pocas estimaciones empíricas de depresión endogámica y heterosis en el mismo sistema para especies cleistógamas. MÉTODOS: Investigamos los costos potenciales de la autofecundación cuantificando la depresión endogámica y la heterosis en tres poblaciones de la perenne cleistógama Ruellia humilis Nutt (Acanthaceae). Realizamos autopolinizaciones manuales, y cruces dentro y entre poblaciones, Medimos el número de semillas, la germinación, la producción total de flores y estimamos la acumulación de fitness para la progenie resultante en un experimento de invernadero. Encontramos depresión endogámica moderada para fitness acumulado (<30%) en dos poblaciones, pero depresión exogámica para cruces dentro de la tercera población (-26%). Entre cruces de población, hubo heterosis de débil a modesta (11-47%) en dos de las combinaciones de poblaciones, pero depresión exogámica moderada a fuerte (-21 a -71%) en las otras cuatro combinaciones. Ni la depresión endogámica, ni la heterosis fueron de suficiente magnitud para explicar la producción continua de flores casmógamas dada la ventaja energética relativa de las flores cleistógamas previamente estimadas para estas poblaciones. La depresión exogámica, ya sea dentro o entre poblaciones, hace que el mantenimiento de las flores casmógamas sea aún más difícil de explicar. Se necesita más información sobre la base genética de la cleistogamia para resolver este enigma.

Autres résumés

Type: Publisher (spa)
Lo que mantiene los sistemas de apareamiento mixto aún es un enigma. La cleistogamia, la producción de flores con potencial de cruzamiento casmógamas, y de flores cleistógamas obligadamente autofecundadas en la misma planta, es un excelente sistema para estudiar los costos de la autofecundación. La depresión endogámica puede prevenir la evolución hacia una mayor autofecundación dentro de las poblaciones, y la heterosis de los cruces entre poblaciones puede inclinar aún más la balanza a favor del cruzamiento. Existen pocas estimaciones empíricas de depresión endogámica y heterosis en el mismo sistema para especies cleistógamas. MÉTODOS: Investigamos los costos potenciales de la autofecundación cuantificando la depresión endogámica y la heterosis en tres poblaciones de la perenne cleistógama Ruellia humilis Nutt (Acanthaceae). Realizamos autopolinizaciones manuales, y cruces dentro y entre poblaciones, Medimos el número de semillas, la germinación, la producción total de flores y estimamos la acumulación de fitness para la progenie resultante en un experimento de invernadero.

Identifiants

pubmed: 37672596
doi: 10.1002/ajb2.16240
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e16240

Informations de copyright

© 2023 The Authors. American Journal of Botany published by Wiley Periodicals LLC on behalf of Botanical Society of America.

Références

Ågren, J., and D. W. Schemske. 1993. Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and B. semiovata. Evolution 47: 125-135.
Anderson, D., and D. Hedgecock. 2010. Inbreeding depression and growth heterosis in larvae of the purple sea urchin Stronglyocentrotus purpuratus (Stimpson). Journal of Experimental Marine Biology and Ecology 384: 68-75.
Ansaldi, B. H., J. J. Weber, C. Goodwillie, and S. J. Franks. 2019. Low levels of inbreeding depression and enhanced fitness in cleistogamous progeny in the annual plant Triodanis perfoliata. Botany 97: 405-415.
Barmentlo, S. H., P. G. Meirmans, S. H. Luijten, L. Triest, and J. G. B. Oostermeijer. 2018. Outbreeding depression and breeding system evolution in small, remnant populations of Primula vulgaris: consequences for genetic rescue. Conservation Genetics 19: 545-554.
Baskin, C. C., and J. M. Baskin. 2014. Seeds: ecology, biogeography, and evolution of dormancy and germination. 2nd ed. Academic Press, San Diego, California.
Bennington, C. C., and W. V. Thayne. 1994. Use and misuse of mixed model analysis of variance in ecological studies. Ecology 75: 717-722.
Busch, J. W. 2006. Heterosis in an isolated, effectively small, and self-fertilizing population of the flowering plant Leavenworthia alabamica. Evolution 60: 184-191.
Byers, D. L., and D. M. Waller. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics 30: 479-513.
Charlesworth, B. 1992. Evolutionary rates in partially self-fertilizing species. The American Naturalist 140: 126-148.
Charlesworth, B. 2018. Mutational load, inbreeding depression and heterosis in subdivided populations. Molecular Ecology 27: 4991-5003.
Charlesworth, D., and B. Charlesworth. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237-268.
Charlesworth, D., and B. Charlesworth. 1995. Quantitative genetics in plants: The effect of the breeding system on genetic variability. Evolution 49: 911-920.
Charlesworth, D., and J. H. Willis. 2009. The genetics of inbreeding depression. Nature Reviews Genetics 10: 783-796.
Cheptou, P. O. 2018. Does the evolution of self-fertilization rescue populations or increase the risk of extinction? Annals of Botany 123: 337-345.
Cheptou, P. O., and K. Donohue. 2011. Environment-dependent inbreeding depression: its ecological and evolutionary significance. New Phytologist 189: 395-407.
Clo, J., and Ø. H. Opedal. 2021. Genetics of quantitative traits with dominance under stabilizing and directional selection in partially selfing species. Evolution 75: 1920-1935.
Clo, J., J. Ronfort, and L. Gay. 2021. Fitness consequences of hybridization in a predominantly selfing species: insights into the role of dominance and epistatic incompatibilities. Heredity 127: 393-400.
Coates, D. J., J. F. Sampson, and C. J. Yates. 2007. Plant mating systems and assessing population persistence in fragmented landscapes. Australian Journal of Botany 55: 239-249.
Cooper, E. S., M. A. Mosher, C. M. Cross, and D. L. Whitaker. 2018. Gyroscopic stabilization minimizes drag on Ruellia ciliatiflora seeds. Journal of The Royal Society Interface 15: 20170901.
Crow, J. F. 1948. Alternative hypotheses of hybrid vigor. Genetics 33: 477-487.
Culley, T. M. 2000. Inbreeding depression and floral type fitness differences in Viola canadensis (Violaceae), a species with chasmogamous and cleistogamous flowers. Canadian Journal of Botany 78: 1420-1429.
Culley, T. M., and M. R. Klooster. 2007. The cleistogamous breeding system: a review of its frequency, evolution, and ecology in angiosperms. The Botanical Review 73: 1-30.
Dudash, M. R. 1990. Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44: 1129-1139.
Eckstein, R. L., and A. Otte. 2005. Effects of cleistogamy and pollen source on seed production and offspring performance in three endangered violets. Basic and Applied Ecology 6: 339-350.
Edmands, S. 1999. Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53: 1757-1768.
Escobar, J. S. N., A. Nicot, and P. David. 2008. The different sources of variation in inbreeding depression, heterosis and outbreeding depression in a metapopulation of Physa acuta. Genetics 180: 1593-1608.
Eyre-Walker, A., and P. D. Keightley. 2007. The distribution of fitness effects of new mutations. Nature Reviews Genetics 8: 610-618.
Fenster, C. B., and L. F. Galloway. 2000. Population differentiation in an annual legume: genetic architecture. Evolution 54: 1157-1172.
Fernald, M. L. 1945. Ruellia in the eastern United States. Rhodora 47: 47-63.
Fisher, R. A. 1941. Average excess and average effect of a gene substitution. Annals of Eugenics 11: 53-63.
Galloway, L. F., T. Cirigliano, and K. Gremski. 2002. The contribution of display size and dichogamy to potential geitonogamy in Campanula americana. International Journal of Plant Sciences 163: 133-139.
Gimond, C., R. Jovelin, S. Han, C. Ferrari, A. D. Cutter, and C. Braendle. 2013. Outbreeding depression with low genetic variation in selfing Caenorhabditis nematodes. Evolution 67: 3087-3101.
Glémin, S. 2003. How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57: 2678-2687.
Glémin, S., and J. Ronfort. 2013. Adaptation and maladaption in selfing and outcrossing species: new mutations versus standing variation. Evolution 67: 225-240.
Goodwillie, C., S. Kalisz, and C. G. Eckert. 2005. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution, and Systematics 36: 47-79.
Harder, L. D., and S. C. H. Barrett. 1995. Mating cost of large floral displays in hermaphrodite plants. Nature 373: 512-515.
Harkness, A., and Y. Brandvain. 2019. The evolutionary response of mating system to heterosis. Journal of Evolutionary Biology 32: 476-490.
Hartfield, M., T. Bataillon, and S. Glémin. 2017. The evolutionary interplay between adaptation and self-fertilization. Trends in Genetics 33: 420-431.
Heywood, J. S., J. S. Michalski, B. K. McCann, K. J. Andres, A. R. Hall, A. D. Hartman, T. C. Middleton, et al. 2022. The potential for floral evolution in response to competing selection pressures following the loss of hawkmoth pollination in Ruellia humilis. American Journal of Botany 109: 1875-1892.
Heywood, J. S., J. S. Michalski, B. K. McCann, A. D. Russo, K. J. Andres, A. R. Hall, and T. C. Middleton. 2017. Genetic and environmental integration of the hawkmoth pollination syndrome in Ruellia humilis (Acanthaceae). Annals of Botany 119: 1143-1155.
Hodgins, K. A., and S. Yeaman. 2019. Mating system impacts the genetic architecture of adaptation to heterogeneous environments. New Phytologist 224: 1201-1214.
Husband, B. C., and D. W. Schemske. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 54-70.
Jump, A. S., R. Marchant, and J. Peñuelas. 2009. Environmental change and the option value of genetic diversity. Trends in Plant Science 14: 51-58.
Karron, J. D., R. J. Mitchell, K. G. Holmquist, J. M. Bell, and B. Funk. 2004. The influence of floral display size on selfing rates in Mimulus ringens. Heredity 92: 242-248.
Lande, R. 1985. The fixation of chromosomal rearrangements in a subdivided population with local extinction and colonization. Heredity 54: 323-332.
Lande, R., and E. Porcher. 2015. Maintenance of quantitative genetic variance under partial self-fertilization, with implications for evolution of selfing. Genetics 200: 891-906.
Lande, R., and D. W. Schemske. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39: 24-40.
Latta, R., and K. Ritland. 1994. Conditions favoring stable mixed mating systems with jointly evolving inbreeding depression. Journal of Theoretical Biology 170: 15-23.
Lippman, Z. B., and D. Zamir. 2007. Heterosis: revisiting the magic. Trends in Genetics 23: 60-66.
Lloyd, D. G. 1979. Some reproductive factors affecting the selection of self-fertilization in plants. The American Naturalist 113: 67-79.
Lohr, J. N., and C. R. Haag. 2015. Genetic load, inbreeding depression, and hybrid vigor covary with population size: An empirical evaluation of theoretical predictions. Evolution 69: 3109-3122.
Long, R. W., and L. J. Uttal. 1962. Some observations on flowering in Ruellia (Acanthaceae). Rhodora 64: 200-206.
Lord, E. M. 1981. Cleistogamy: a tool for the study of floral morphogenesis, function and evolution. The Botanical Review 47: 421-449.
Lynch, M. 1991. The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45: 622-629.
Manzitto-Tripp, E. A., and T. F. Daniel. 2023. Phylogeny and revised classification of New World Ruellia. Taxon. Website: https://doi.org/10.1002/tax.13001 [in press].
Marr, A. B., L. F. Keller, and P. Arcese. 2002. Heterosis and outbreeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia). Evolution 56: 131-142.
Munguía-Rosas, M. A., M. J. Campos-Navarrete, and V. Parra-Tabla. 2013. The effect of pollen source vs. flower type on progeny performance and seed predation under contrasting light environments in a cleistogamous herb. PLoS One 8: e80934.
Muyle, A., H. Martin, N. Zemp, M. Mollion, S. Gallina, R. Tavares, A. Silva, et al. 2020. Dioecy is associated with high genetic diversity and adaptation rates in the plant genus Silene. Molecular Biology and Evolution 38: 805-818.
Oakley, C., J. Ågren, and D. W. Schemske. 2015a. Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana. Heredity 115: 73-82.
Oakley, C. G., S. Lundemo, J. Ågren, and D. W. Schemske. 2019. Heterosis is common and inbreeding depression absent in natural populations of Arabidopsis thaliana. Journal of Evolutionary Biology 32: 592-603.
Oakley, C. G., K. S. Moriuchi, and A. A. Winn. 2007. The maintenance of outcrossing in predominantly selfing species: ideas and evidence from cleistogamous species. Annual Review of Ecology, Evolution, and Systematics 38: 437-457.
Oakley, C. G., J. P. Spoelhof, and D. W. Schemske. 2015b. Increased heterosis in selfing populations of a perennial forb. AoB Plants7: plv122. https://doi.org/10.1093/aobpla/plv122
Oakley, C. G., and A. A. Winn. 2008. Population-level and family-level inbreeding depression in a cleistogamous perennial. International Journal of Plant Sciences 169: 523-530.
Oakley, C. G., and A. A. Winn. 2012. Effects of population size and isolation on heterosis, mean fitness, and inbreeding depression in a perennial plant. New Phytologist 196: 261-270.
Opedal, Ø. H., W. S. Armbruster, T. F. Hansen, A. Holstad, C. Pélabon, S. Andersson, D. R. Campbell, et al. 2023. Evolvability and trait function predict phenotypic divergence of plant populations. Proceedings of the National Academy of Sciences USA 120: e2203228120.
Paland, S., and B. Schmid. 2003. Population size and the nature of genetic load in Gentianella germanica. Evolution 57: 2242-2251.
Rathcke, B. J., and E. S. Jules. 1993. Habitat fragmentation and plant-pollinator interactions. Current Science 65: 273-277.
Schierup, M. H., and F. B. Christiansen. 1996. Inbreeding depression and outbreeding depression in plants. Heredity 77: 461-468.
Seguí, J., S. Hervías-Parejo, and A. Traveset. 2021. Selective forces on the maintenance of outcrossing in an almost exclusively cleistogamous violet species. American Journal of Botany 108: 2452-2463.
Sheridan, P. M., and D. N. Karowe. 2000. Inbreeding, outbreeding, and heterosis in the yellow pitcher plant, Sarracenia flava (Sarraceniaceae), in Virginia. American Journal of Botany 87: 1628-1633.
Soto, T. Y., N. A. Ryan, and C. G. Oakley. 2023. Relative energetic economy of cleistogamous selfing in three populations of the perennial Ruellia humilis. International Journal of Plant Sciences. Website: https://doi.org/10.1086/727456 [in press].
Stojanova, B., S. Maurice, and P. O. Cheptou. 2016. Is plasticity across seasons adaptive in the annual cleistogamous plant Lamium amplexicaule? Annals of Botany 117: 681-691.
Stojanova, B., S. Maurice, and P. O. Cheptou. 2020. Season-dependent effect of cleistogamy in Lamium amplexicaule: flower type origin versus inbreeding status. American Journal of Botany 107: 155-163.
Stojanova, B., Z. Münzbergová, and H. Pánková. 2021. Inbreeding depression and heterosis vary in space and time in the serpentinophyte perennial Minuartia smejkalii. Preslia 93: 149-168.
Toczydlowski, R. H., and D. M. Waller. 2023. Failure to purge: population and individual inbreeding effects on fitness across generations of wild Impatiens capensis. Evolution 77: 1315-1329.
Uyenoyama, M. K., and D. M. Waller. 1991. Coevolution of self-fertilization and inbreeding depression I. Mutation-selection balance at one and two loci. Theoretical Population Biology 40: 14-46.
Vogler, D. W., and S. Kalisz. 2001. Sex among the flowers: The distribution of plant mating systems. Evolution 55: 202-204.
Volis, S., I. Shulgina, M. Zaretsky, and O. Koren. 2011. Epistasis in natural populations of a predominantly selfing plant. Heredity 106: 300-309.
Waller, D. M. 2021. Addressing Darwin's dilemma: can pseudo-overdominance explain persistent inbreeding depression and load? Evolution 75: 779-793.
Weller, S. G., A. K. Sakai, D. A. Thai, J. Tom, and A. E. Rankin. 2005. Inbreeding depression and heterosis in populations of Schiedea viscosa, a highly selfing species. Journal of Evolutionary Biology 18: 1434-1444.
Whitehead, M. R., R. Lanfear, R. J. Mitchell, and J. D. Karron. 2018. Plant mating systems often vary widely among populations. Frontiers in Ecology and Evolution 6. https://doi.org/10.3389/fevo.2018.00038
Whitlock, M. C., P. K. Ingvarsson, and T. Hatfield. 2000. Local drift load and the heterosis of interconnected populations. Heredity 84: 452-457.
Winn, A. A., E. Elle, S. Kalisz, P. O. Cheptou, C. G. Eckert, C. Goodwillie, M. O. Johnston, et al. 2011. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution 65: 3339-3359.
Winn, A. A., and K. S. Moriuchi. 2009. The maintenance of mixed mating by cleistogamy in the perennial violet Viola septemloba (Violaceae). American Journal of Botany 96: 2074-2079.

Auteurs

Tatyana Y Soto (TY)

Department of Botany and Plant Pathology and the Center for Plant Biology, Purdue University, West Lafayette, IN, USA.

Juan Diego Rojas-Gutierrez (JD)

Department of Botany and Plant Pathology and the Center for Plant Biology, Purdue University, West Lafayette, IN, USA.

Christopher G Oakley (CG)

Department of Botany and Plant Pathology and the Center for Plant Biology, Purdue University, West Lafayette, IN, USA.

Articles similaires

Female Oocytes Animals Ovary Mice
Animals Animal Migration Swimming Japan Seasons

Evidence for inbreeding depression in captive Damaraland mole-rats.

David Seager, Amy E Leedale, Jack Benjamin Thorley et al.
1.00
Animals Mole Rats Female Inbreeding Depression Male
Animals Oxidative Stress Female Reproduction Immunocompetence

Classifications MeSH