How plant populations keep a genetic memory of the past

Jewelweed is found throughout eastern parts of North America. By studying jewelweed, researchers can understand how environmental changes affect plants over time. (Liz West), CC BY Plants are usually seen as stationary life forms, quietly supporting environments. But plant communities and populations are far from static. They are constantly being shaped by the world around them. One way is through local extinction — the loss of a local population from a specific patch of landscape. Another is through local colonization — the spreading or returning of plants to a landscape patch. In fact, many plant species are thought to be composed of metapopulations, which are sets of local populations connected by colonization, local extinction and population growth across a landscape. If we were able to observe a metapopulation on the landscape over a time-lapse film covering several hundred years, we might see how the metapopulation changes and evolves as the film unfolds. Of course, no such film exists, and time machines have not yet been invented, so understanding the forces that determine the history of metapopulations remains a challenge. So, how can researchers understand the history of plant metapopulations? To do this, my colleague Rachel Toczydlowski and I turned to DNA sequence data with the plant jewelweed, or as botanists call it, Impatiens capensis. Tracking wildlife using DNA: A scientific breakthrough made with an Indigenous community

What is jewelweed? Jewelweed is found throughout eastern parts of North America, including southern Québec and Ontario, and into the midwestern United States. This annual plant can form seeds through both cross-fertilization in normal flowers and through self-fertilization via a special type of closed flower that botanists refer to as a cleistogamous flower. Self-fertilization allows a single dispersing individual plant to establish a new population because it does not require a mate.

The plant has the ability to found new populations from one or a few individuals via self-fertilization. The theory of metapopulations predicts that jewelweed as a species should be composed of a highly dynamic metapopulation where some patches have only been recently colonized, while others have been so for longer periods. Jewelweed is typically found today in the forest fragments left over after agricultural and urban development. This type of habitat once existed as more continuous forest cover that blanketed much of the eastern and middle parts of North America prior to European colonization. This is especially true of the area in Wisconsin where we conducted our study, which is mostly farmland today, but retains island-like patches of more natural habitat. Our research We analyzed DNA sequence information obtained by sequencing the genomes of individual members of the population, and focused on how the individual genomes differ from one another. Lining up the sequences and comparing them reveals differences in the DNA sequences of a sample of plants called single nucleotide polymorphisms (SNPs). These are positions in the sequence that differ from one another by possessing different nucleotides, the individual components of the sequence. We then looked at the site frequency spectrum of each population, which shows how many SNPs are rare, how many are common and how many fall in between. Population founding events can change how common different SNPs are. When a new population is founded by only a few individuals, many SNPs end up occurring at moderate frequencies. If the population then grows rapidly, new SNPs appear by mutation but remain rare, which changes the overall pattern of genetic variation. And so, the form of the site frequency spectrum provides a kind of “genetic memory” of demographic events that gave rise to the individual-component plant populations within the metapopulation that we see today. By applying this technique to DNA sequence data, we were able to detect significant differences in the demographic histories of the populations sampled. Some populations appeared to have only recently been founded and from a few individuals, whereas others appeared to be larger and more stable. This pattern fits what is predicted by metapopulation theory for a species whose plants are capable of self-fertilization. The younger populations also exhibited loss of genetic diversity and higher levels of inbreeding compared to the older, more stable populations, which contained more diversity and were less inbred. The higher inbreeding in younger populations suggests that they were founded by very few individuals and have not yet had enough time or gene flow from neighbouring populations to rebuild genetic diversity. Importance for conservation

Genetic variability is the foundation of adaptation. High levels of inbreeding can lead to weak or damaging traits being passed on to new generations, which reduces the health of populations. From a conservation standpoint, higher levels of diversity and lower levels of inbreeding are often desirable attributes. They can enhance the adaptability and stability of populations, something that is becoming increasingly important as the climate changes. Complicating our understanding of metapopulations, however, is the fact that not all landscapes are created equal. Some are more prone than others to disturbance and recovery, and when it comes to colonization of landscapes, not all plant species are created equal. For instance, plants that can self-pollinate are more capable of founding a population from a few individuals and may be especially good colonizers compared with plants that require mates for seed production. Understanding metapopulation history provides conservation managers with an additional perspective, especially when it comes to selecting the healthiest populations to conserve. We may not have a time machine, but by analyzing the DNA of living populations, we can uncover the echoes of the past and understand their genetic implications for conservation.

Daniel J Schoen receives funding from the Natural Sciences and Research Council of Canada.