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Ecological Effects on Estimates of Effective Population Size in an Annual Plant

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Ecological Effects on Estimates of Effective Population Size in an Annual Plant Biological Conservation 143 (2010) 946–951 Contents lists available at ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon Ecological effects on estimates of effective population size in an annual plant E.K. Espeland a,*, K.J. Rice b a USDA ARS Pest Management Research Unit, 1500 N. Central Avenue, Sidney, MT 59270, USA b Ecology Graduate Group, Department of Plant Sciences, Mail Stop 1, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA article info abstract Article history: Effective population size (Ne) is a critical indicator of the vulnerability of a population to allele loss via Received 13 April 2009 genetic drift, and it can also be used to assess the evolutionary potential of a population. While some Received in revised form 28 December 2009 plant conservation plans have focused on outcrossing through cross-pollination as a way to increase esti- Accepted 3 January 2010 mated N , variance in reproductive output determined by ecological factors such as competition can also Available online 25 January 2010 e strongly affect estimated Ne. We examined the effects of intraspecific and interspecific competition, stressful soils, and local adaptation on estimates of Ne in an annual plant species. While ecological influ- Keywords: ences on plant growth rate variance have been predicted to influence estimates of N /N, we found a sig- Abiotic stress e nificant effect on the estimate of N /N, but no significant ecological effects on growth rate variance. Lower Competition e Effective population size survivorship on stressful soil was the most important effect reducing estimates of Ne/N. If stochastic mor- Genetic drift tality is greater in environments that are abiotically stressful, then populations in these stressful environ- Plantago erecta ments may be slower to adapt because of lower census sizes and reduction of Ne/N. In populations of Local adaptation conservation concern, increasing survivorship may be of greater benefit for maximizing Ne than the Serpentine reduction of variability in reproductive output among surviving adults. Conservation genetics Ó 2010 Elsevier Ltd. All rights reserved. 1. Introduction (Lande, 1988; Frankham, 1995; Hedrick, 1995; Frankham et al., 2003), many of which are ecological in nature. Effective population size (Ne) can be used to assess the evolu- Published estimates of Ne in plant populations have most often tionary potential of a population because it is an important indica- been used in a descriptive manner to characterize population sub- tor of the vulnerability of a population to allele loss through division and differentiation (Tremblay and Ackerman, 2001; Latta, random processes (genetic drift). A population with a very low 2008). Conservation biologists working with both plants and ani- Ne is more susceptible to genetic drift and less able to respond to mals have used Ne estimates to explore the importance of popula- selection. This is because in small populations there is less genetic tion bottlenecks on genetic diversity (Frankham, 1995; Amos and variation for natural selection to act upon, and there is a higher Harwood, 1998). Other conservation uses of Ne estimates have fo- probability that beneficial alleles will not be maintained by selec- cused on reconstructions of historical anthropogenic effects on tion and will instead be lost from the population because of gene flow and genetic diversity (Levy and Neal, 1999; Morris random drift effects (Willi et al., 2007). Modeling population ge- et al., 2002). netic processes in conservation has become relatively widespread Ne can be estimated in a number of ways, and there are three (Halley and Manasee, 1993; Higgins and Lynch, 2001; Obioh and commonly-used types of Ne. Inbreeding Ne describes the probabil- Isichei, 2007; Pertoldi et al., 2007; Palstra and Ruzzante, 2008), ity of mating among relatives, therefore lowering genetic diversity and when Ne is incorporated into minimum viable population size of the population. Variance Ne describes the probability that indi- (MVP) models, MVP as censused may need to be substantially viduals will pass on their genes to the next generation, with in- more than 5000 individuals (Obioh and Isichei, 2007). Rare and creased variance in offspring number leading to a decrease in Ne. endangered plant populations in particular often have very low Extinction or eigenvalue Ne describes the rate of loss of heterozy- census sizes (N) and even lower estimated Ne (Chung et al., 2007; gosity, with a calculation of an asymptotic Ne as the outcome. Zietsman et al., 2008). Plant and animal populations of conserva- Although estimates of the three types of Ne often have the same re- tion concern tend to have multiple factors acting to reduce Ne sult (Vitalis and Couvet, 2001), they can differ, so the choice of which type to calculate may revolve around the genetic process of interest (Caballero, 1994). Inbreeding Ne is often estimated via * Corresponding author. Tel.: +1 406 433 9416; fax: +1 406 433 5038. genetic methods by calculating the percent heterozygosity and E-mail addresses: [email protected] (E.K. Espeland), kjrice@ucdavis. comparing it to the expected heterozygosity in the population if edu (K.J. Rice). 0006-3207/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2010.01.003 E.K. Espeland, K.J. Rice / Biological Conservation 143 (2010) 946–951 947 it were in equilibrium (Hartl and Clark, 2007). Inbreeding Ne can resource distribution reduces the CV of plant sizes as densities in- also be estimated as the geometric mean of population sizes crease (Koide and Dickie, 2002). This would lead to a relative in- through time (Caballero, 1994). Variance Ne is estimated as the var- crease in estimated Ne /N when seed output is positively iance in reproductive outputs among individuals in a population correlated with plant size. (Heywood, 1986). Published estimates of Ne /N for annual plants In this experiment we used populations of the California native tend to be between 5% and 30%, with ratios most often below annual forb, Plantago erecta (E. Morris), to examine environmental 10% (Heywood, 1986; Husband and Barrett, 1992; Goldringer and evolutionary influences on variance in reproductive output et al., 2001; Siol et al., 2007). and estimated Ne. We designed the experiment to test the relative Recent work by Siol et al. (2007) suggests that relative repro- importance of density-dependent interactions and interspecific ductive variance must be taken into account in order to correctly competition on reproductive hierarchies, and how stressful soils estimate Ne. As understanding of the influence of reproductive var- and local adaptation may alter estimates of Ne/N. iance on Ne estimation has increased, evidence has also accumu- lated to demonstrate that ecological factors can be extremely important in determining this variance (Van Kleunen et al., 2001, 2. Methods and materials 2005). In fact, ecological models of density-dependence have al- ready been theoretically extended to the estimation of Ne (Rice, P. erecta is an annual plant with a native range extending from 1990; Koide and Dickie, 2002; Van Kleunen et al., 2001, 2005). Baja California and Arizona north through the California Floristic Other ecological factors such as herbivory (Doak, 1992) can affect Province to southern Oregon. Although completely self-compati- the variance in reproductive outputs in plants and thus influence ble, some outcrossing is likely in this species (E. Espeland, unpub- estimates of Ne/N. Although Ne is often estimated from the geomet- lished data). Populations of P. erecta typically occur at high ric mean of population sizes of above-ground plants, seed banks in- densities and are found in shallow, low fertility soils (e.g., serpen- crease Ne above this estimate because the seed bank is often not tine outcrops, road cuts) as well as in deep, more fertile grassland part of the censused population size (Nunney, 2002). Thus, ecolog- soils. ical factors that reduce the seed bank such as granivory and fungal The experiment was conducted at McLaughlin Reserve infection will act to reduce Ne. (38.52°N, 122.24°W), located within the California North Coast The linkage between variation in reproductive output and Range (Hickman, 1993) and operated by the University of Califor- estimates of Ne in annual plants was explored theoretically by nia Natural Reserve System. Seeds were collected from the field Heywood (1986) and can be expressed by the following in spring 2004 from four serpentine populations and four non-ser- relationship: pentine populations at McLaughlin Reserve. Serpentine soil is a nutrient-limited, ultramafic soil type characterized by low calcium, Ne 1 very high levels of exchangeable magnesium (Jurjavcic et al., 2002), ¼ ð1Þ N ½ð1 þ FÞðr2=l2Þþ1 and toxic heavy metals: a stressful environment for plant growth (Kruckeberg, 1984). Serpentine areas are also often drier than where the inbreeding coefficient F ranges from 0 (complete out- non-serpentine areas (Macnair et al., 1989). Serpentine popula- crossing) to 1 (complete inbreeding), r2 = variance in reproductive tions of P. erecta were identified by the presence of serpentine en- output, and l = mean reproductive output. It follows that if an an- demic plant species. Serpentine grasslands occur in a mosaic with nual plant population with a large census size has a few individuals loam grasslands at this site. Four populations on each soil type that produce the majority of the seed, reproductive variance is high within a geographic range of three linear kilometers were selected and estimated Ne/N is small. In contrast, Ne is larger and estimated to span a range of productivities (estimated by total above-ground Ne/N is close to 1 in an annual plant population of large census size biomass; E. Espeland, unpublished data) and were spatially that has a variance in reproductive output that approximates a Pois- blocked into serpentine/loam paired plots.
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