Elsevier

Aquatic Toxicology

Volume 95, Issue 1, 19 October 2009, Pages 71-79
Aquatic Toxicology

Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna

https://doi.org/10.1016/j.aquatox.2009.08.004Get rights and content

Abstract

Provided that gene flow is not too high, selection by local environmental conditions in heterogeneous landscapes can lead to genetic adaptation of natural populations to their local habitat. Pollution with anthropogenic toxicants may create pronounced environmental gradients that impose strong local selection pressures. Toxic contaminants may also directly impact genetic structure in natural populations by exhibiting genotoxicity or by causing population declines resulting in genetic bottlenecks. Using populations of Daphnia magna established from the dormant egg banks of ponds located in a landscape dominated by anthropogenic impact, we aimed at detecting evidence for local adaptation to environmental contamination. We explored the relationship between land use around the 10 investigated ponds, population genetic diversity as measured by neutral genetic markers (polymorphic allozymes) and the tolerance of the populations originating from these ponds to acute lethal effects of two model toxicants, the pesticide carbaryl and the metal potassium dichromate. Genetic diversity of the populations as observed by neutral markers tended to be negatively impacted by agricultural land use intensity (Spearman rank correlation, R = −0.614, P = 0.059), indicating that genetic bottlenecks may have resulted from anthropogenic impact. We experimentally observed differences in susceptibility to both carbaryl and potassium dichromate among the studied pond populations of D. magna (analysis of deviance, P < 0.001). Because the experimental design excluded the possibility of physiological adaptation of the test animals to the toxicants, we conclude that the differences in susceptibility must have a genetic basis. Moreover, carbaryl tolerance levels of the populations tended to increase with increasing agricultural land use intensity as described by ranked percentage of land coverage with cereal and corn crop in the proximity of the ponds (Spearman rank correlation, R = 0.602, P = 0.066). Together, these two findings provide evidence for local adaptation of D. magna populations to pesticide contamination. Overall, the results demonstrate the potential selection pressure imposed by anthropogenic pollution and provide evidence that genetic erosion in natural Daphnia populations is related to anthropogenic impact.

Introduction

Natural populations are exposed to a variety of spatially and temporarily changing selection pressures. Under certain conditions, including sufficiently strong environmental gradients and the absence of high levels of gene flow, genetic adaptation of populations may occur in response to local selection pressures. Such local adaptation leads to a higher average fitness of a resident population in the local habitat compared to conspecifics from other habitats (Kawecki and Ebert, 2004). Specifically in freshwater zooplankton, the observation of high levels of genetic differentiation among neighbouring populations despite the high dispersal capacity of the organisms was explained by the fitness advantage of locally adapted populations over immigrants, resulting in low effective gene flow (De Meester et al., 2002). Local adaptation has been detected in many species in relation to various environmental stressors (Reznick and Ghalambor, 2001). In the freshwater crustacean Daphnia magna Straus, local adaptation in behaviour and life history traits has for example been reported with regard to predation pressure (De Meester, 1996a, Boersma et al., 1999, Cousyn et al., 2001).

It is expected that populations can also locally adapt to other stressors such as exposure to anthropogenic pollutants (De Meester, 1996b). Reznick and Ghalambor (2001) summarize in their review cases of insecticide and herbicide tolerance in animals and plants. The occurrence of metal-tolerant invertebrates in metal-polluted environments is a well documented phenomenon (Morgan et al., 2007). In many studies, however, distinguishing between physiological acclimatization and genetic differences between individuals indicating adaptation is not possible because organisms are tested immediately after field collection rather than performing tests with offspring of the isolated organisms after culturing them in the absence of the suspected stressor in a common environment for several generations (Morgan et al., 2007). Yet, Lopes et al., 2005, Lopes et al., 2006 provided evidence for both physiological acclimatization and genetic adaptation in populations of freshwater crustaceans to heavy metal contamination.

One pre-requisite for local adaptation to a specific stressor to occur, is the presence of sufficient genetic variation within local populations, with genotypes differing in their susceptibility to the stressor. In D. magna, genetic differences between clones in susceptibility to acutely lethal effects of toxicants have been reported for heavy metals such as cadmium and hexavalent chromium (Baird et al., 1991) and for pesticides such as the organophosphorus insecticides ethyl parathion (Barata et al., 2001) and fenitrothion (Damasio et al., 2007). Yet, local adaptation to such toxicants has rarely been investigated in field populations of Daphnia. Potential local adaptation was indicated for ethyl parathion, where Barata et al. (2000) detected greater survival upon pesticide exposure in a field population represented by 50 clones compared to uniclonal laboratory populations. Whereas no genetic differences in cadmium tolerance were detected among populations in that study (Barata et al., 2000), Barata et al. (2002a) observed in another study with four D. magna field populations significant among-population differences in susceptibility to cadmium.

The genetic variation within natural populations and, hence, the potential for local adaptation can itself be impacted by anthropogenic pollution. Mutagenic pollutants can increase genetic variation, albeit mostly creating deleterious mutations, and toxic pollutants can lead to impoverishment of genetic diversity by causing genetic bottlenecks due to population collapses (Hebert and Luiker, 1996, Bickham et al., 2000). Moreover, if adaptation to one specific stressor results in a reduction of genetic diversity, this may in turn lead to the population being less resistant to a multi-stressor environment (Depledge, 1994). A reduction of genetic diversity within a population does not only impact the potential for evolutionary adaptation, but may also directly lead to decreased fitness through inbreeding effects (Hebert and Luiker, 1996, Haag et al., 2005). Finally, reduced genetic diversity may lead to the fixation of deleterious alleles in the population during demographic bottlenecks and thereby further reduce fitness in a process termed mutational meltdown (Lynch et al., 1995). There is good evidence that reduced genetic diversity is associated with increased susceptibility to parasites and pathogens (Ladle, 1992). In analogy, populations with reduced genetic diversity may show higher susceptibility to anthropogenic pollutants, as was reported for cadmium tolerance in Chironomus riparius populations following inbreeding (Nowak et al., 2008).

The aim of the present study was to investigate the relationship between genetic diversity and toxicant tolerance in natural populations of D. magna, and to document potential evidence for local genetic adaptation to anthropogenic pollution as represented by two model pollutants (hexavalent chromium and carbaryl). We particularly hypothesized that the tolerance of Daphnia populations for carbaryl would be positively correlated with the presence of acetylcholinesterase-inhibiting pesticides in their habitat. Lacking actual pesticide monitoring data for the investigated ponds, we used land use patterns around the ponds as a proxy for pesticide contamination.

Section snippets

Sampling and background of D. magna populations

Since the pioneering work of Hebert (reviewed in Hebert, 1978, De Meester et al., 2006), D. magna has been proven an excellent study organism in population genetics. In addition, Daphnia is also well established as a standard test species in ecotoxicology. Under favourable conditions D. magna reproduces by amictic parthenogenesis, whereas environmental cues associated with unfavourable conditions will trigger sexual reproduction. The sexually produced eggs are dormant eggs, encapsulated by a

Genetics of the investigated populations

Population Mo was polymorphic at three of the screened loci and fixed for one allele at the locus Pgi, whereas all other populations were polymorphic at all four loci. The characteristics of the genetic structure of the 10 investigated populations are given in Table 2. Population Mo had a lower allelic richness than the other populations at two loci and also showed rather low genetic diversity, with an expected heterozygosity (He) of 0.243 compared to a He ranging from 0.369 to 0.528 in the

Discussion

The genetic diversity (He) as observed among hatchlings of the dormant egg banks of the studied populations ranged from 0.208 to 0.515. This is in line with earlier studies on active populations in shallow eutrophic ponds in the same region (Vanoverbeke et al., 2007). The He observed here is higher than values found in dormant populations of small rock pools (Korpelainen, 1986), which might be due to the larger and more stable habitat provided by the ponds studied here. Genetic diversity in

Acknowledgements

This research was supported by a postdoctoral fellowship grant from the K.U. Leuven to A.C. and by K.U. Leuven project OT/04/23 and FWO project G.00229.09. We thank Cathy Duvivier and Wendy van Doorslaer for providing the sediment sample of pond #10. Thanks to Christian Ritz for giving key advice on plotting the fitting curves in R.

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