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Predicting Heterosis and Inbreeding Depression from Population Size and Density to Inform Management Efforts

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Received: 10 January 2020 | Accepted: 27 March 2020 DOI: 10.1111/1365-2664.13643 RESEARCH ARTICLE Predicting heterosis and inbreeding depression from population size and density to inform management efforts Linus Söderquist | Anna Broberg | Viktor Rosenberg | Nina Sletvold Plant Ecology and Evolution, Department of Ecology and Genetics, Evolutionary Abstract Biology Centre, Uppsala University, Uppsala, 1. Effective population size should be positively related to census size and den- Sweden sity, and it is expected to influence the strength of genetic drift, inbreeding Correspondence and response to selection, and thus the distribution of the genetic load across Linus Söderquist Email: [email protected] populations. 2. We examined whether census population size and density predict the strength of Funding information Svenska Forskningsrådet Formas, Grant/ inbreeding depression, heterosis and population mean fitness at the seed stage Award Number: 2014-601 in the terrestrial orchid Gymnadenia conopsea by conducting controlled crosses Handling Editor: Jin-Tian Li (self, outcross within and between populations) in 20 populations of varying size (7–30,000 individuals) and density (1–12.8 individuals/m2). In the largest popula- tion, we also examined how local density affects the occurrence of self-pollination with a pollen staining experiment. 3. The majority of populations expressed strong inbreeding depression at the seed stage (mean δID: min–max = 0.26: −0.53 to 0.51), consistent with a mainly out- crossing mating system and substantial genetic load. The effect of between- population crosses varied from strong outbreeding depression to heterosis (mean δOD: min–max = 0.05: −0.22 to 0.92), indicating varying influence of drift and selection among populations. 4. Census population size did not significantly predict the strength of inbreeding depression, heterosis or population mean fitness. However, inbreeding depression was positively and heterosis negatively correlated with population density. The proportion of self-massulae deposition was three times higher in sparse patches compared to dense ones (41% vs. 14%). 5. Combined effects of density-dependent pollinator behaviour and limited seed dispersal may cause stronger genetic sub-structuring in sparse populations and reduce the strength of the correlation between census and effective population size. The results point to the importance of considering population density in addi- tion to size when evaluating the distribution of recessive deleterious alleles across populations. 6. Synthesis and applications. Management plans for threatened species often involve crosses between populations to restore genetic variation, a process termed genetic This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Journal of Applied Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society J Appl Ecol. 2020;57:1459–1468. wileyonlinelibrary.com/journal/jpe | 1459 1460 | Journal of Applied Ecology SÖDERQUIST et AL. rescue. This study indicates that such conservation efforts should be more successful if designed on the basis of population density in addition to population size, because we found population density predicted both the strength of hetero- sis and inbreeding depression across populations of Gymnadenia conopsea. KEYWORDS density-dependent mating, genetic rescue, Gymnadenia conopsea, heterosis, inbreeding depression, population density, population size, selfing rate 1 | INTRODUCTION selection decreases (Lynch & Gabriel, 1990). Beneficial alleles may be lost via random drift, and inbreeding can lead to exposure of During the last century, many species have experienced significant recessive deleterious alleles that cause inbreeding depression reductions in abundance and local population sizes due to habitat (i.e. inbreeding load; Husband & Schemske, 1996). The strength of degradation and fragmentation (Ceballos, Ehrlich, & Dirzo, 2017; inbreeding depression should be weaker in small relative to large Sánchez-Bayo & Wyckhuys, 2019). A reduction in population size is populations because the inbreeding load should be reduced by ge- expected to lead to increased extinction risk and lowered adaptation netic drift (Hedrick & García-Dorado, 2016). Drift is expected to potential (Leimu & Fischer, 2008). Hence, the census size of a pop- randomly fix mildly deleterious alleles (and lose strongly deleterious ulation is regularly used as a measure of its viability, and it is an im- ones), reducing the difference in expression of recessive deleterious portant determinant of a species' conservation value in management alleles between progeny resulting from selfing versus outcrossing. decisions (IUCN, 2012). How suitable census size is as a measure of Closer kinship due to biparental inbreeding in small populations will a species' conservation value will depend on its correspondence to also contribute to diminished differences between outcrossing and effective population size, determined by the number of individuals selfing. Additionally, inbreeding load can be reduced by selection that actually contribute offspring to the next generation, and the against alleles when expressed as homozygotes (Keller & Waller, equality of their contributions (Wright, 1938). 2002). However, the removal of deleterious alleles through selection In most natural populations, census population size will be (i.e. purging) requires a relatively large population size to be effec- larger than effective population size, as not all adult individuals tive, and should mainly act on strongly deleterious alleles (García- breed. More interesting from a conservation viewpoint is that pop- Dorado, 2015; Winn et al., 2011). Fixation of deleterious alleles via ulations of equal census size can differ in several ways influencing drift and inbreeding can ultimately reduce population fitness and effective population size. One factor that may strongly affect the lead to a decrease in adaptation potential (Ellstrand & Elam, 1993; mating structure and thereby the effective size is population den- Young, Boyle, & Brown, 1996), increasing the extinction probability sity (Levin, 1988). In flowering plants, several studies have docu- of small populations (Whitlock, 2000). mented density-dependent pollinator behaviour, where pollinators Besides reducing population size, habitat fragmentation typ- visit fewer plants (Kunin, 1997) and more flowers per plant at low ically also leads to increased isolation. The combination of re- density relative to high (Grindeland, Sletvold, & Ims, 2005; Karron, duced gene flow and increased inbreeding and genetic drift will Thumser, Tucker, & Hessenauer, 1995). Density-dependent be- lead to stronger genetic differentiation between populations haviour should lead to shorter pollen dispersal distances, more (Templeton, Shaw, Routman, & Davis, 1990). As deleterious al- geitonogamy and lower outcrossing rates (Karron et al., 1995; Peter leles are fixed at random by genetic drift, different populations & Johnson, 2009), and stronger fine-scale genetic structure in can, by chance, fix different alleles (Keller & Waller, 2002). sparse populations (or patches) compared to dense ones (reviewed in In such cases, between-population crosses can restore het- Loveless & Hamrick, 1984; Vekemans & Hardy, 2004). For example, erozygosity and lead to increased fitness, that is, heterosis spatial aggregation was found to increase the magnitude of genetic (Crow, 1948; Whitlock, Ingvarsson, & Hatfield, 2000). Heterosis structuring within natural populations of Silene ciliata (Lara-Romero is expected to be strongest in small populations, where random et al., 2016). Knowledge of density-dependent mating patterns is fixation of mildly deleterious alleles should be common (Oakley important for understanding the correspondence between census & Winn, 2012; Spigler, Theodorou, & Chang, 2017). Crosses and effective population size, and ultimately for guiding the design between small populations can thus be used as a conservation of conservation plans. effort, that is, genetic rescue (Ingvarsson, 2001, reviewed in Effective population size influences many ecological and genetic Frankham, 2015). However, populations can also be adapted to processes. Small populations typically have low levels of genetic differing local conditions, where between-population crosses variation (Leimu, Mutikainen, Koricheva, & Fischer, 2006). The in- would lead to outbreeding depression, that is, lowered fitness fluence of genetic drift and inbreeding also increases in small pop- as compared to within-population outcrossing (Oakley, Ågren, & ulations (Ellstrand & Elam, 1993), whereas the efficiency of natural Schemske, 2015; Templeton et al., 1986). As small populations SÖDERQUIST et AL. Journal of Applied Ecolog y | 1461 are expected to show low potential for local adaptation (Leimu & Fischer, 2008), the strength of outbreeding depression is pre- dicted to increase with population size. To separate the inbreed- ing and drift load across populations, it is important to combine knowledge on the strength of inbreeding depression versus het- erosis (Keller & Waller, 2002). Low inbreeding depression and no heterosis indicate a history of purging of deleterious alleles, whereas low inbreeding depression and high heterosis imply that drift is the dominating process determining
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