Genes rolling down the river

Sarah Shainker wrote this post as a part of Dr. Stacy Krueger-Hadfield’s Conservation Genetics course at the University of Alabama at Birmingham. Sarah completed a B.S. in Marine Biology at the College of Charleston before serving as a Peace Corps volunteer in the Philippines, where she developed interests in environmental education and communicating science to conservation and management stakeholders. She is currently a first-year PhD student and a Blazer Fellow and NSF GRFP Fellow in the Krueger Hadfield lab. She plans to integrate population genetics and a citizen science monitoring network to develop eco-evolutionary studies of freshwater macroalgae in the riverscapes of the southeast United States. 

Genes travel on land, in rivers, and through the sea

Landscape genetics combines population genetics, landscape ecology, and spatial structure to study the influence of the environment on genetic population structure. The field originated, as you can probably glean from the name, through the study of terrestrial species.

As terrestrial organisms ourselves, it’s not too difficult to imagine the forces that may restrict or promote dispersal and gene flow. Increasing geographic distances between populations are expected to correspond with genetic isolation. Landscape features like rivers, mountain ranges, or patches of deforested land may create discrete barriers between populations. Continuous variables like rainfall or temperature create resistance which may slow down dispersal and gene flow. 

As the field of landscape genetics has grown to include aquatic and marine organisms, we’ve learned that our expectations of what genetic patterns look like across space do not always translate neatly to seascapes and riverscapes. There are some key differences in the lifestyles and challenges of organisms inhabiting different environments. Distinct hypotheses have therefore been developed to explain genetic variation in seas and rivers (Davis et. al., 2018).

Marine organisms are more likely than their terrestrial counterparts to cover a larger geographic range, perhaps leading to the presumption that there would be little differentiation among their populations. However, many seascape genetics studies have focused on marine invertebrates, which are more accessible for sampling than mobile species, such as migratory fish or marine mammals.

These organisms often reproduce through external fertilization and disperse during larval, planktonic life stages, during which they are at the mercy of currents. It is infeasible to track the movement of larvae over large distances over time, but particle tracking models combined with oceanographic data on characteristics such as currents, temperature, and chlorophyll content can help us identify pathways and barriers to gene flow. Hypotheses generated by models and physical oceanographic data can be tested by comparing them to empirical genetic data. For example, we can test for correlations of population isolation with geographic distance by using sea distance, defined as the shortest possible pathway through water without crossing land. This choice would be similar to that of testing for isolation by geographic distance on land; however, a more biologically relevant analysis may be to test for Isolation by Oceanographic Distance, defined as the shortest possible path of dispersal based on oceanographic data (Jahnke et al., 2017).

Riverscapes have their own unique implications for population structure. Freshwater organisms inhabit complex, branching networks of rivers and streams with unidirectional water flow, to which gene flow is confined (Davis et. al., 2018). There are discrete barriers like waterfalls and dams, as well as barriers in the form of environmental characteristics such as temperature, precipitation, water depth and velocity, and light availability. These characteristics can shift spatially throughout the network, as well as over seasons or longer timescales (Vannote et. al., 1980). 

The influence of the riverscape

There are a slew of hypotheses about how the unique characteristics of the riverscape influence the diversity and distribution of organisms within them. The River Continuum Concept views the river as a highly variable environment, where the biological community maintains stability. This theory predicts that evolution will select for energy efficiency, and that peak species diversity will occur at confluences because of downstream increases in the diversity of aquatic insects countered by upstream increases in the diversity of snails and mollusks (Vannote et. al., 1980). 

The Mighty Headwaters Hypothesis (Finn et. al., 2011) predicts that populations of small headwaters and tributaries will harbor highly differentiated and diverse biological communities at both the inter- and intra-species levels, while the Stream Hierarchy Model (Meffe & Vrigenhoek, 1988) predicts that the high amount of habitat fragmentation within river networks will lead to isolation by distance along the network. The characteristic of unidirectional water flow suggests a Downstream Increase in Genetic Diversity (DIGD). Paz-Vinas et al., (2015) combined a meta-analysis with simulations to find that this trend was generally true across species, but showed a weaker pattern among overland dispersers compared to species that disperse through water.

Why real-world patterns are more complex than models

While these hypotheses are useful starting points for understanding the influence of environment on gene flow and population structure, it turns out that their applicability and relevance varies depending on the biology of the species in question. An organism’s dispersal mechanisms, reproductive strategy, and habitat preferences interact with the riverscape to shape population structure and genetic diversity. Biological characteristics can be used to make predictions on genetic structure; likewise, patterns found in genetic data can be used to make predictions and inferences about species biology. Interactions among genetics, biology, and environment can surely vary enough to create countless scenarios!

A study of the round rocksnail, a threatened freshwater mussel in the southeast US, found that its population structure supported both DIGD and the Stream Hierarchy Model’s prediction of isolation by distance within the stream network. However, patterns did not support the upstream movement of gastropods suggested by the River Continuum Concept, nor the Mighty Headwaters Hypothesis (Whelan et. al., 2018). 

Riparian plants were expected to follow the pattern of DIGD because their seeds are known to be spread by the unidirectional flow of water. However, adherence to this pattern has not been as strong as expected, suggesting that zoochory (animal-based seed dispersal) may play a larger role than suspected by carrying seeds upstream (Hevroy et. al., 2018). The landscape barriers and corridors to bird movement may therefore have a larger impact than expected on the riverscape structure of riparian plants. Studies of riparian plants have also shown that reproductive strategy can play a role in population structure: Pollux et al., (2007) found that environmental heterogeneity shapes reproductive variability which shapes genetic diversity and population structure.

Although we may expect mobile taxa to be resistant to environmental and geographic influences, it appears they are not completely immune to influences of the riverscape. Kanno et al., (2011) found that a species of brook trout followed weak IBD patterns within streams and that genetic clustering correlated with stream confluences as barriers. This pattern is partially due to the unidirectional flow of water within branching networks, and partially due to species biology. Although brook trout actively disperse, they don’t swim far from home; and although dominant individuals displace subordinate individuals, the displaced individuals don’t travel very far either.

The complexity of patterns observed show us that we can’t predict population structure based on either environmental hypotheses or species biology alone. In order to more fully explain population structure of river and stream-dwellers, studies should incorporate ecological and geographic knowledge of the riverscape with the biology and natural history of the organisms that live there. Future studies on organisms covering a variety of life history strategies, combined with their genetic data, will help us to unravel population genetic patterns that emerge from interactions between a variety of biota in a variety of environments.

Fig. 4 “The handsomest of our game fishes”, Salvelinus fontinalis

References

Davis, CD, Epps, CW, Flitcroft, RL, & Banks, MA (2018). Refining and defining riverscape genetics: How rivers influence population genetic structure. WIREs Water 5: e1269, doi: 10.1002/wat2.1269.

Finn, DS, Bonada, N, Murria, C, & Hughes, JM (2011). Small but mighty: headwaters are vital to stream network biodiversity at two levels of organization. J. N. Am. Benthol. Soc 30(4): 963-980. doi: 10.1899/11-012.1.

Hevroy TH, Moody ML, & Krauss SL (2018). Population enetic analysis reveals barriers and corridors for gene flow within and among riparian populations of a rare plant. AoB PLANTS 10:plx065; doi:10.1093/aobpla/plx065.

Jahnke, M, Jonsson, PR, Moksnes, P, Loo, L, Jacobi, MN, Olsen, JL (2018). Seascape genetics and biophysical connectivity modelling support conservation of the seagrass Zostera marina in the Skagerrak-Kattegat region of the eastern North Sea. Evolutionary Applications 11: 645-661. doi: 10.1111/eva.12589.

Kanno, Y, Vokoun, J, & Letcher, B (2011). Fine-scale population structure and riverscape genetics of brook trout (Salvelinus fontinalis) distributed continuously along headwater channel networks. Molecular Ecology 20 (18):3711-3729. doi: 10.1111/j.1365-294X.2011.05210.x

Meffe, GK & Vrijenhoek, RC (1988). Conservation genetics in the management of desert fishes. Conservation Biology (2): 157-169.

Paz-Vinas I, Loot G, Stevens VM, & Blanchet S (2015). Evolutionary processes driving spatial patterns of intraspecific genetic diversity in river ecosystems. Molecular Ecology 24: 4586-4604. doi: 10.1111/mec.13345.

Pollux, BJA, Jong, MDE, Steegh, A, Verbruggen, E, Van Groenendael, JM, & Ouborkg, NJ (2007). Reproductive strategy, clonal structure and genetic diversity in populations of the aquatic macrophyte Sparganium emersum in river systems. Molecular Ecology 16, 313-325. doi: 10.1111/j.1365-294X.2006.03146.x

Vannote, RL, Minshall, GW, Cummins, KW, Sedell, JR, & Cushing, CE (1980). The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences 37: 130-137.

Whelan NV, Galaska MP, Sipley BN, Weber JM, Johnson PD, Halanych KM, & Helms BS (2019). Riverscape genetic variation, migration patterns, and morphological variation of the threatened Round Rocksnail, Leptoxis amplaMolecular Ecology 28, 1593-1610. doi: 10.1111/mec.15032.

About Stacy Krueger-Hadfield

I am a marine evolutionary ecologist interested in the impacts of seascapes and complex life cycles on marine population dynamics. I use natural history, manipulative field experiments and population genetic and genomic approaches with algal and invertebrate models in temperate rocky shores,estuaries and the open ocean.
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