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Behind the science: Looking for the population genetic signatures of variable clonality across an environmental gradient

About the author: Will H. Ryan is a postdoc currently working in the Krueger-Hadfield Lab at the University of Alabama at Birmingham on the evolutionary ecology of marine organisms with complex life cycles. In order to better understand mechanisms driving local adaptation and life cycle diversity, he studies how environmental variation interacts with genetic and plastic trait variation to shape geographic patterns in growth, sexual and asexual reproduction, and genetic structure. Check out his work on his website.



Our contribution (Ryan et al. 2021) to the recent special issue on Sexual and Asexual reproduction is, in many ways, the victory flag planted at the top of a long sought-after summit. My work with the clonal sea anemone Diadumene lineatabegan in 2011 when I started reading about a species I had stumbled upon in a tidepool in Massachusetts while helping a friend with fieldwork a few months before (Figure 1). I had just entered a PhD program intending to study the effect of environmental variation on the structure of the community of protists and invertebrates that colonize the liquid inside Purple Pitcher Plants (Sarracenia purpurea).  Yet, after reading a few articles about D. lineata, I was utterly taken by what I imagined could be discovered with this charming little sea anemone. This species is presumed native to East Asia and likely spread initially through oyster trade in the 19thcentury (Verrill 1898). Interestingly, these anemones had been shown to increase their rate of clonality with temperature (Minasian 1979), though the consequences of this phenomenon had not been placed in either a biogeographic or seasonal context. In this species’ remarkable success as an invader, I saw the potential for experimental tests of many of the hypotheses that have been put forth to explain the adaptive value of clonal life cycles.

Figure 1. Diadumene lineata in a Massachusetts tidepool in 2010. This is the picture that launched my quest to study life cycle evolution with this anemone. (WH Ryan CC-BY-NC)

Luckily, I was blessed with a VERY understanding advisor in Dr. Tom Miller (Florida State University), who encouraged (humored?) my exploration of this unexpected left turn. A decade later, this work has taken me around the world and put thousands of miles on my car tracing the coastal outline of the United States, all in search of a clearer understanding of the causes and consequences of living a partially clonal lifestyle. But really, as is so often true in science, reaching this waypoint has only allowed us a clearer view of the Everest of questions that loom ahead.

In the special issue article (Ryan et al. 2021), we identified clonemates and estimated other metrics of genetic structure using newly developed genetic markers, which has broadened the range of questions we can address. While microsatellites markers can feel like old news in an era of routine genome-scale sequencing, the data generated by these reliable and affordable (once developed) markers are a revelation for understanding clonal biology. The need to develop molecular tools to address questions about the evolution of clonality with this species was obvious from the start, but reaching that goal took time. As a PhD student I fumbled through a process of microsatellite development for the species, but lacked the guidance and resources to develop an adequate set of markers. As a postdoc, I have been lucky to continue working in this system alongside other projects. With the expertise of Dr. Stacy Krueger-Hadfield and help of a fantastic undergraduate researcher, Jaclyn Aida, we were able to finally able to unlock this achievement.

We demonstrated that environmentally-mediated variation in fission rate and gamete production correlated with predictable latitudinal patterns of genetic diversity and clone size across the Atlantic range of the non-native sea anemone Diadumene lineata (Figure 2). In my doctoral research, I showed that genetic and plastic variation in the rate of binary fission produced a latitudinal gradient in expected clonal expression on the Atlantic Coast, such that southern populations divide far more frequently than northern populations (Ryan 2018). Seasonal temperature variation within a site drives an alternating pattern of life cycle expression where individuals grow large in the spring, followed by a rapid reduction in individual body size through fission in the heat of the summer (Ryan 2018). Geographic and seasonal changes in body size related to fission rate plasticity also correspond to differences in the timing and magnitude of gametogenesis, across the Atlantic range (Ryan and Miller 2019). In our Journal of Heredity paper, we supported a hypothesis that emerged from my dissertation findings – namely, that expected local patterns of fission and gamete production leave a clear signal in the genetic structure at a site.

Figure 2. (A) The number of individuals per genet (the collective term for all clonally derived individuals of the same genotype) at 8 sites across the Atlantic Coast latitudinal range of D. lineata. Sites are paired within region – left to right: Florida (CML, WAK), Georgia (STS, JEK), Virginia (RBB, QBY), Massachusetts (NAH, PMH). The latitudinal pattern is captured by (B) comparing the Pareto β index (a measure of how evenly ramets are distributed among genets) over the increasing mean annual water temperature from north to south. (Ryan et al. 2021)

The existence of a feedback loop between clonal behavior and standing genetic structure is a critical assumption of theory that seeks to explain life cycle variation via eco-evolutionary consequences. For example, the strawberry-coral model (Williams 1975) posits that partially clonal life cycles evolve to exploit the expected benefits of both asexual and sexual reproduction in spatially complex environments. It suggests that clonal growth is advantageous for dominating a local patch where a particular genotype is well suited, whereas genetically diverse offspring produced through recombination and gamete exchange are needed for founding new, environmentally unique patches. The benefits of clonal investment are realized when ramets (the word for individual representatives of a clonal lineage) outcompete sexually derived offspring for space in a local patch. Implicit in this explanation is the assumption that the reproductive investment strategies employed by individuals will result in characteristic spatial arrangements of genetic diversity – that is, highly clonal genotypes will fill the local environment with their clonal progeny, while sexually produced propagules will travel far from the natal patch.

For sea anemones however, the connection between reproductive mode and spatial organization is not necessarily straightforward. Sea anemone adults are capable of wandering around (albeit slowly, from our perspective) and/or drifting on the current (Bedgood et al. 2020). Little is known (so far) about the dispersal habits of sea anemone larvae, though their larval duration tends to be short. Both of these facets of anemone biology may reduce the benefits of partial clonality envisioned by Williams (1975) in the strawberry-coral model. Furthermore, differences in mortality from predation, disturbance or stress across the species range could counterbalance geographic differences in clonal investment such that the standing size of clones does not differ among sites. Thus, for any species, a link between expected reproductive investment and genetic structure needs to be empirically demonstrated before it can be invoked to support a theoretical explanation. In the case of our study, the clonal genetic structure of D. lineata populations along the Atlantic Coast largely matched our expectations based on variation in clonal and gametogenic behavior. However, our results also hinted that habitat type (e.g., rockpools vs. oyster reef vs. human infrastructure, etc.) may play a complicating role in shaping the size and spatial distribution of clones. Our ongoing projects will help define the contributions of theses interacting influences.

Figure 3. Diadumene lineata come in several color morphs. Characteristic patterns appear to be faithfully maintained by clonal descendants; thus, the size of a patch of similarly patterned individuals might be a clue to the size of a clone. However, anemones with different genotypes can produce similar color patterns. The classic unpaired-orange-stripe morph (left) is the most common. We lovingly refer to the pattern on the right as the “gentleman’s pajamas” morph, for its striking resemblance to pinstriped fabric. (WH Ryan CC-BY-NC)

The challenge now is to use the molecular tools and natural history knowledge we have developed for D. lineatato examine a broader array of patterns and processes that likely shape investment in clonal and sexual reproduction. For example, the roles of body-size-mediated metabolism and gamete production have emerged as critical elements for understanding the adaptive value of fission behavior (Ryan et al. 2019), tying together genetic and energetic explanations for the evolution of clonality. Picking apart the push and pull of genetic and energetic costs and benefits that shape local adaptation in life cycle expression will likely fill up our next decade or more. In addition, documenting patterns of gene flow and connectivity at regional and continental scales, including within the native range, will help us better distinguish patterns of adaptive differentiation from differences that arose through historical accident. Finally, describing the contours of how D. lineata expanded across the globe will help us parse the tangled influences of history, environment, and mating system that are driving contemporary life cycle evolution and local adaptation in this species. Hopefully, these details will help us better understand the adaptive landscapes that other marine species will face when confronted with novel environments.



Bedgood SA, Bracken MES, Ryan WH, Levell ST, Wulff JL. 2020. Environmental drivers of adult locomotion and reproduction in a symbiont- hosting sea anemone. Mar Biol. 167. Article no. 39.

Minasian LL. 1979. The effect of exogenous factors on morphology and asexual reproduction in laboratory cultures of the intertidal sea anemone, Haliplanella luciae (Verrill) (Anthozoa: Actiniaria) from Delaware. J Exp Mar Biol Ecol. 40:235–246.

Ryan WH. 2018. Temperature-dependent growth and fission rate plasticity drive seasonal and geographic changes in body size in a clonal sea anemone. Am Nat. 191:210–219.

Ryan WH, Adams L, Bonthond G, Mieszkowska N, Pack KE, Krueger- Hadfield SA. 2019. Environmental regulation of individual body size con- tributes to geographic variation in clonal life cycle expression. Mar Biol. 166. Article no. 157.

Ryan WH, Aida J, Krueger-Hadfield SA. 2021. The contribution of clonality to population genetic structure in the sea anemone, Diadumene lineata. J Hered.doi:10.1093/jhered/esaa050

Ryan WH, Miller TE. 2019. Reproductive strategy changes across latitude in a clonal sea anemone. Mar. Ecol. Prog. Ser. 611:129–141.

Verrill AE. 1898. Descriptions of new American actinians, with critical notes on other species. Am J Sci. 4:493–498.

Williams GC. 1975. Sex and evolution. Monogr Popul Biol. 8:3–200.

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