To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates

Abstract

Variation in dispersal capacity may influence population genetic variation and relatedness of freshwater animals thus demonstrating how life-history traits influence patterns and processes that in turn influence biodiversity. The majority of studies have focused on the consequences of dispersal variation in taxa inhabiting riverine systems whose dendritic nature and upstream/downstream gradients facilitate characterizing populations along networks. We undertook extensive, large-scale investigations of the impacts of hydrological connectivity on population genetic variation in two freshwater bryozoan species whose dispersive propagules (statoblasts) are either attached to surfaces (Fredericella sultana) or are released as buoyant stages (Cristatella mucedo) and that live primarily in either lotic (F. sultana) or lentic environments (C. mucedo). Describing population genetic structure in multiple sites characterized by varying degrees of hydrological connectivity within each of three (or four) UK regions enabled us to test the following hypotheses: (1) genetic diversity and gene flow will be more influenced by hydrological connectivity in populations of C. mucedo (because F. sultana dispersal stages are retained); (2) populations of F. sultana will be characterized by greater genetic divergence than those of C. mucedo (reflecting their relative dispersal capacities); and (3) genetic variation will be greatest in F. sultana (reflecting a propensity for genetic divergence as a result of its low dispersal potential). We found that hydrological connectivity enhanced genetic diversity and gene flow among C. mucedo populations but not in F. sultana while higher overall measures of clonal diversity and greater genetic divergence characterized populations of F. sultana. We suggest that genetic divergence over time within F. sultana populations reflects a general constraint of releasing propagules that might eventually be swept to sea when taxa inhabit running waters. In contrast, taxa that primarily inhabit lakes and ponds may colonize across hydrologically connected regions, establishing genetically related populations. Our study contributes more nuanced views about drivers of population genetic structures in passively dispersing freshwater invertebrates as outlined by the Monopolization Hypothesis (Acta Oecologica, 23, 2002, 121) by highlighting how a range of demographic and evolutionary processes reflect life-history attributes of benthic colonial invertebrates (bryozoans) and cyclically parthenogenetic zooplankton. In addition, growing evidence that genetic divergence may commonly characterize populations of diverse groups of riverine taxa suggests that organisms inhabiting lotic systems may be particularly challenged by environmental change. Such change may predispose riverine populations to extinction as a result of genetic divergence combined with limited dispersal and gene flow.

Open research badges: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.1tm8705.

Keywords: Cristatella mucedo; Fredericella sultana; dispersal ability; gene flow; hydrological connectivity; statoblasts.

Figure 1

Statoblasts of Cristatella and Fredericella. (a) Senescing Cristatella colony filled with statoblasts enclosed within degrading colony wall at end of growing season (scale bar = 2 mm). Inset shows buoyant, released Cristatella statoblast with hooks at tips of radial spines (scale bar = 0.5 mm). (b) Unadorned and nonbuoyant Fredericella statoblasts (piptoblasts) retained within persistent colony tube (scale bar = 0.5 mm)

Figure 2

Locations of bryozoan samples subject to genetic analysis across the four UK regions (a = Norfolk, b = Cumbria, c = Greater Glasgow, d = Northern Ireland). Cristatella mucedo samples identified by solid triangles (black triangles = Directly Hydrologically Connected sites [DHC]; red triangles = Hydrologically Connected sites [HC]; blue triangles = Isolated [I] sites). Fredericella sultana samples identified by solid circles (black circles = Directly Hydrologically Connected [DHC] sites; blue circles = Isolated [I] sites)

Figure 3

Average values (and n‐values) with standard error bars for parameters that significantly varied with hydrological connectivity (a, b, c) and region (d) in Cristatella mucedo. (a) N _C = mean number of clones; R = mean genotypic richness; (b) H _E = expected heterozygosity; N _A = mean number of alleles; (c) F _ST = genetic differentiation index; M = averaged gene flow estimates (derived from Migrate‐n; Beerli, 2006; Beerli et al., 2009); (d) F _IS = inbreeding coefficient index

Figure 4

Average values (and n‐values) with standard error bars for parameters that significantly varied with region (a, b) and hydrological connectivity (c) in Fredericella sultana. F _ST = genetic differentiation index; N _C = mean number of clones; R = mean genotypic richness; H _O = observed heterozygosity

Figure 5

Regional DAPC plots of local population structure in relation to hydrological connectivity for Cristatella mucedo (a) and Fredericella sultana (b). Plots of genetic relatedness among unique MLGs (small dots) along the first (horizontal) and second (vertical) most significant discriminant axes (DAs). Diamonds and crosses represent, respectively, the centered area of plots for each bryozoan population (identified by population codes; Table S1). Symbol colors signify hydrological connectivity as per key. DHC, Directly Hydrologically Connected; HC, Hydrologically Connected; I, Isolated sites (I) sites. Boxes provide details for region, number of PCAs, and significant discriminant axes (DAs) retained in each plot

Figure 6

General population structure according to DAPC plots for Cristatella mucedo (a) and Fredericella sultana (b). Dot colors reflect the degree of genetic relatedness among samples. Circles outline the main genetic clusters in geographical region (i.e., Norfolk, Cumbria, Glasgow, and Northern Ireland). Boxes provide details for the number of PCAs and significant discriminant axes (DAs) retained included in each plot