The Monopolization Hypothesis and the dispersal–gene flow paradox in aquatic organisms

Abstract

Many aquatic organisms rely on passive transport of resting stages for their dispersal. In this review, we provide evidence pointing to the high dispersal capacity of both animals (cladocerans, rotifers and bryozoans) and aquatic macrophytes inhabiting lentic habitats. This evidence includes direct observation of dispersal by vectors such as wind and waterfowl and the rapid colonization of new habitats. Such high dispersal capacity contrasts with the abundant evidence of pronounced genetic differentiation among neighbouring populations in many pond-dwelling organisms. We provide an overview of the potential mechanisms causing a discrepancy between high dispersal rates and reduced levels of gene flow. We argue that founder events combined with rapid local adaptation may underlie the striking patterns of genetic differentiation for neutral markers in many aquatic organisms. Rapid population growth and local adaptation upon colonization of a new habitat result in the effective monopolization of resources, yielding a strong priority effect. Once a population is locally adapted, the presence of a large resting propagule bank provides a powerful buffer against newly invading genotypes, so enhancing priority effects. Under this Monopolization Hypothesis, high genetic differentiation among nearby populations largely reflects founder events. Phylogeographic data support a scenario of low effective dispersal among populations and persistent effects of historical colonization in cyclical parthenogens. A comparison of patterns of gene flow in taxa with different life cycles suggests an important role of local adaptation in reducing gene flow among populations. We argue that patterns of regional genetic differentiation may often reflect historical colonization of new habitats rather than contemporary gene flow.

Introduction

Inland waters are often isolated from each other, providing an excellent example of island habitats. The resulting isolation is extreme in ephemeral ponds scattered in semi-arid regions, but also holds for streams and rivers belonging to different catchment areas. In addition, these environments offer only ephemeral and/or unpredictable habitats in an intermediate to long-term scale, as most ponds and lakes are geologically short-lived. Aquatic organisms inhabiting inland water bodies have, therefore, to rely on either active flight (many aquatic insects) or passive dispersal mediated by resistant stages (Bilton et al., 2001). In this review, we will focus on organisms inhabiting lentic habitats (lakes and ponds) that disperse passively via resting propagules Cáceres, 1997, Colbourne et al., 1997. These resting stages accumulate in the sediments of their habitats forming resting propagule banks that are in many aspects equivalent to plant seed banks Hairston, 1996, Cáceres and Hairston, 1998. The wide geographical ranges of many aquatic taxa are testimony that passive dispersal by resting stages can be very effective, an observation made by both Lyell (1832) and Darwin (1859).

For a long time, it was thought that many aquatic taxa were essentially cosmopolitan. Mayr (1963), for instance, wrote “...species (of freshwater organisms) that are successful in colonizing temporary bodies of water have in general such superb dispersal abilities that their entire world population may well be nearly panmictic”. Although detailed morphological studies (Frey, 1982) and recent molecular work Colbourne and Hebert, 1996, Schwenk et al., 1998, Gómez et al., 2000 have changed this view dramatically, it remains that many taxa are widespread. In addition, experimental work by Jenkins and Buikema (1998) has provided direct evidence for rapid colonization of newly formed habitats, supporting indirect evidence provided by a variety of more anecdotal records 〚see Bilton et al. (2001) for review〛. However, studies employing neutral genetic markers have often reported strong genetic differentiation among zooplankton populations inhabiting nearby ponds, suggestive of low levels of ongoing gene flow 〚reviewed in Lynch and Spitze, 1994, De Meester, 1996a, and below〛.

We will argue that this apparent paradox of high dispersal and low gene flow can be explained by a combination of stochastic and selection-driven processes that have recently been shown to be particularly effective in populations of several aquatic organisms. First, rapid population growth rates after a historical colonization event from a few founding propagules prevent allele frequency changes due to gene flow (Boileau et al., 1992). The persistent effect of founding events is further enhanced by the presence of very large dormant propagule banks in these organisms Hairston, 1996, Brendonck et al., 2000. In addition, rapid adaptation of resident populations to local conditions strongly reduces effective gene flow among populations De Meester, 1993, De Meester, 1996a, Okamura and Freeland, 2002, thus effectively increasing persistence of founder events. The present contribution integrates these processes into one hypothesis that we have termed ‘the Monopolization Hypothesis’, which can be viewed as an extension of the persistent founder effects hypothesis presented by Boileau et al. (1992).

Our aim is to examine recent findings that are relevant to the Monopolization Hypothesis. We start by critically reviewing studies that provide information concerning dispersal ability versus gene flow in lentic aquatic organisms. We subsequently review and discuss factors and processes that may play a role in solving this dispersal–gene flow paradox: the persistent influence of founding events (Boileau et al., 1992), the buffering against population crashes provided by resting propagule banks, and rapid local adaptation De Meester, 1996a, Okamura and Freeland, 2002. First, we focus on cyclically parthenogenetic zooplankton. In the second part, patterns of gene flow and phylogeography are compared among aquatic taxa that differ in life cycle and investment in sexual reproduction. The comparative survey provides an insight into how the frequency and timing of sexual reproduction, as well as the production of propagules, may influence patterns of genetic differentiation among populations inhabiting ponds and lakes.