Manipulating evolution to conserve species

Sarah Fitzpatrick fishing for guppies in Trinidad.

This post is by MSU Postdoc Sarah Fitzpatrick working at the Kellogg Biological Station

Consider a native fish population in a small headwater stream with low genetic diversity due to genetic drift and founder effect (loss of variation that occurs when a new population is established by a small number of individuals). High levels of inbreeding occur because most individuals in this population are close relatives. A dam is put in downstream, erasing the chance of occasional natural connectivity and gene flow from a different population. Drainage from an upstream agricultural plot slowly leaks a toxic pesticide into the stream. Imagine your job is to keep this natural resource—the native fish population—alive and healthy. What’s your plan?

I study evolution through the lens of conservation (and vice versa). How can we manipulate our understanding of ‘evolution in action’ in order to buy time for imperiled populations and facilitate adaptation during rapid environmental change?

Dry intermittent reaches like what is pictured here in Big Sandy Creek prevent connectivity among fish populations.

Humans and climate change have modified natural connectivity patterns of many organisms, producing dire consequences for some. When populations become isolated they tend to be more vulnerable to risks associated with small population size. Combined with further habitat loss and environmental disturbance, this perfect storm of risk factors can culminate in dramatic population decline. We are faced with many situations similar to the scenario I described above. Ninety-three percent of vertebrate species listed under the U.S. Endangered Species Act exist in fragments from a formerly connected range.

I’ve mostly thought about this question in the context of freshwater fish populations that live in headwater streams. Headwater environments make fascinating natural laboratories for studying evolution in the wild because 1) multiple replicate populations often exist across neighboring streams; 2) headwater-restricted populations tend to be isolated from the homogenizing effects of gene flow and have high potential for local adaptation; but 3) they are often colonized by one or several individuals, experience strong genetic drift, and may need occasional gene flow to adapt and persist.

From a conservation perspective, headwater environments are incredibly important yet fragile ecosystems that harbor high biodiversity and are threatened by pollution, physical barriers like dams, and drying from groundwater removal or drought.

Both of the fish species I will highlight from my research occur in small headwater populations, yet they tell quite different stories. My goal is to link the evolutionary biology we’ve learned about one to the conservation biology and management plan of the other. The first is the Trinidadian guppy, an invasive species on six continents, but also a textbook example for studying rapid evolution in the wild (Magurran 2005). The second is the Arkansas darter, a Great Plains endemic in steep decline, and a candidate for listing under the Endangered Species Act.

In Trinidad we took advantage of experimental guppy translocation experiments (Travis et al. 2014) to test the effects of gene flow from divergent populations on locally adapted traits, fitness, and population dynamics in native downstream populations. First, we found evidence for high and rapid gene flow downstream from all six historical introduction sites, yet guppies maintained locally important trait differences that we know to be adaptive based on extensive previous work in the system (Fitzpatrick et al. 2015). Then, we focused on two native populations from headwater tributaries that were downstream from the most recent translocations. We began studying these populations before the introductions and gene flow took place and found that these native populations had tiny effective population sizes (Ne = 2-10) and were likely experiencing inbreeding (Fitzpatrick et al. 2016).

Male guppies from the mark-recapture monitoring project

Gene flow began as non-native guppies swam or were washed downstream and began mating with the native guppies. Our field team visited the two focal populations each month for two and a half years and caught all guppies over 14 mm (about the width of your thumbnail) using traps, mask and snorkel, and butterfly nets. All fish each month were weighed and photographed and all new recruits to the population were given a unique colored tattoo under a microscope and had three scales removed for genetic analyses before being returned to their exact site of capture. In total, over 10,000 guppies from the two streams were individually marked, monitored throughout their lifetimes, and could be classified using molecular markers as a pure native guppy, a pure immigrant, or a hybrid. This study was novel in its ability to capture the initial and long-term effects of gene flow on survival and population dynamics in replicated populations in the wild.

Thick black lines indicate total number of guppies > 14mm captured in each stream over time. Grey boxes correspond to the timeframe in which every individual was genotyped at microsatellite loci for classification into genetic ancestry groups. Colors show the number of individuals in each genetic group caught each month.

Despite gene flow from guppy populations that were originally divergent and adapted to a different environment, genetic rescue (an increase in fitness caused by the introduction of new genetic variation) was documented in both streams. Monthly population sizes skyrocketed from under one hundred to over one thousand individuals, genetic diversity increased substantially, and importantly, much of the success could be attributed to hybrid guppies ( Fitzpatrick et al. 2016).

The types of experiments and monitoring we were able to accomplish in Trinidad are simply not an option for a threatened species like the Arkansas darter. However, the small, native guppy populations we studied could be thought of as proxies for other genetically isolated, imperiled populations. For example, we know that Arkansas darters exist in small, genetically isolated populations and that drought and groundwater removal are causing populations to become even more fragmented (Fitzpatrick et al. 2014). Given the increasing consensus that genetic rescue works, under the right conditions (Whiteley et al. 2015; Frankham 2015; Fitzpatrick et al. 2016), I argue that a management plan involving assisted gene flow is worth serious consideration.

But, many unknowns remain. Deciphering the grey area of when gene flow is needed to increase fitness and provide a demographic boost versus when it results in homogenization, or worse, reduces fitness through introducing maladaptive alleles, is a major challenge. Model systems for studying ‘evolution in action’, like the Trinidadian guppy, might become increasingly crucial for conservation if understanding and manipulating evolutionary processes indeed proves to be one way to curb unprecedented rates of biodiversity loss.

Fitzpatrick, S. W., Gerberich, J. C., Angeloni, L. M., Bailey, L. L., Broder, E. D., Torres-Dowdall, J., Handelsman, C. A., López-Sepulcre, A., Reznick, D. N., Ghalambor, C. K. and W.C. Funk. (2016), Gene flow from an adaptively divergent source causes rescue through genetic and demographic factors in two wild populations of Trinidadian guppies. Evolutionary Applications. doi: 10.1111/eva.12356
Fitzpatrick SW, Crockett H, Funk WC (2014) Water availability strongly impacts population genetic patterns of an imperiled Great Plains endemic fish. Conservation Genetics, 15, 771–788.
Fitzpatrick SW, Gerberich JC, Kronenberger JA, Angeloni LM, Funk WC (2015) Locally adapted traits maintained in the face of high gene flow. Ecology Letters, 18, 37–47.
Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Molecular Ecology, 24, 2610–2618.
Magurran AE (2005) Evolutionary ecology: the Trinidadian guppy. Oxford University Press, Oxford.
Travis J, Reznick D, Bassar RD et al. (2014) Do Eco-Evo Feedbacks Help Us Understand Nature? Answers From Studies of the Trinidadian Guppy. Advances in Ecological Research, 50, 1–40.
Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends in Ecology & Evolution, 30, 42–49.

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