Evolution in a common landscape: a tale of two stickleback species

All species cope to some extent with environmental heterogeneity. How do they achieve this? Do they tolerate or avoid extreme conditions? Or do they adjust to local selective environments through adaptive evolution? Many studies in evolutionary ecology look into these questions one species at the time. Yet, species do not live in isolation, but are assembled in communities. We might thus ask if members of the same community respond to environmental conditions similarly or in species-specific ways. Answering this question is important for understanding the eco-evolutionary dynamics of communities. Since anthropogenic impact on natural systems may simultaneously put multiple species at risk, a multi-species approach is also relevant for conservation and natural resource management. In a new article in Nature Communications, we investigate to what extent two stickleback species, the threespine stickleback and its relative the ninespine stickleback, evolve “collectively” across contrasting environments. That is, a tale of two stickleback species in a common landscape.

Evolutionary biologists have accumulated ample evidence for contemporary evolution in natural populations. Meanwhile, the question of why populations do (or do not) evolve and whether they evolve in a predictable manner will still keep us busy for quite some time. There are many species and many environmental contexts in which species can evolve. For as much as we know, the way populations evolve is species- and context-dependent – and thus highly variable. This is reflected in meta-analyses such as in last month’s issue of the American Naturalist, where Krista, Gregor, Caroline and Andrew illustrated that even when we expect populations to evolve in a predictable direction (i.e., parallel evolution), the extent to which they actually do so is highly variable (Oke et al 2017). Across species and environmental contexts, populations thus show anything from “very” parallel to “not-so-parallel” evolution. Aspects of evolution are thus not very predictable.

Things become clearer when focusing on one species at the time. One of the species that has been strongly fueling the debate of the importance of parallel and non-parallel evolution is threespine stickleback. Indeed, of the 92 studies included in Krista-and-friends’ meta-analysis, 26 studies featured this very species. One of the most convincing, wide-spread and best understood cases of evolution in nature is the rapid parallel evolution of reduced body armour (e.g. from high to low numbers of lateral plates and from long to short spines) when marine threespine stickleback populations colonize freshwater. Importantly, these populations often evolve in a predictable manner, but we also have a fairly good understanding for why they sometimes don’t. Gene flow, for instance, which homogenizes the gene pool and therefore slows down or halts adaptive divergence, explains some of the limits on the evolution towards low-plated populations in freshwater (Raeymaekers et al 2014). In another threespine stickleback ecotype pair, the lake-stream system, variation in phenotypic and genomic parallelism could not only be explained by gene flow, but also by the magnitude of the difference between the lake and stream environment, which has an amplifying effect on adaptive divergence (Stuart et al 2017). Studies like this generate a better mechanistic understanding of evolution, because they show how strong selection on ecologically relevant traits and their underlying genes has to be to contribute to local adaptation, and how often there is a common genetic basis for such traits.

Threespine stickleback populations can evolve rapidly from completely plated (top) to low-plated (bottom), while homogenising gene flow can slow down this process, even when selection on plate number is evident from one generation to the next (Raeymaekers et al 2014). Photo credit: Anna Mazzarella.

Yet, single-species studies hold a major limitation for the study of contemporary evolution in nature: they do not provide insight in the generality of contemporary evolution. For instance, the evolutionary versatility of threespine stickleback may be exceptional, and thus levels of adaptation in this species may be not representative of the typical strength of adaptation in nature. And of course, species do not live in isolation but are assembled in communities. Members of the same community often face similar environmental gradients, but do not necessarily respond similarly to these gradients. From a community perspective, it is important to understand the variation in these responses, in particular because adaptation to local selective environments in one species may also influence adaptation in other species (e.g. through competition or dilution effects). So, in order to fully understand biodiversity patterns across ecologically diverse landscapes, we should consider multiple interacting species simultaneously, providing a more holistic view on the landscape processes shaping biodiversity. This also makes sense for conservation and natural resource management, since anthropogenic impact on natural systems may simultaneously put multiple species at risk.

In our new study, we performed a comparison between the threespine stickleback and its relative the ninespine stickleback (Raeymaekers et al 2017). We primarily wanted to find out to what extent both species differ in evolutionary potential to deal with challenges along the broad habitat gradient over which they coexist. In western Europe, both species co-occur frequently at the exact same spots, which includes both freshwater and brackish habitats. Yet, both species also have a wide-spread geographic distribution, are closely related (allowing us to compare homologous traits and genomic regions), show interesting differences in ecology, and are highly abundant, and thus represent an excellent pair of species for this type of study. We sampled both species at four freshwater sites and four brackish sites, and then compared them for various aspects of population divergence. We analysed 1) whether the two species show phenotypic and genomic signatures of adaptive divergence along environmental gradients, 2) to what extent both species show parallel patterns of population divergence, and 3) what are the most important spatial and environmental drivers of population divergence in each species.

“Von dem Stichling”. Description of threespine and ninespine stickleback in “Fischbuch: das ist ein kurtze, doch vollkommene Beschreybung aller Fischen so in dem Meer und süssen Wasseren…” by Gessner and Forer (Zürich, 1563).With two and six dorsal spines, the drawings of both species do not look very professional. Yet, even nowadays the number of spines is a source of confusion. Threespine stickleback sometimes have four spines, and in Dutch the ninespine stickleback is called “tiendoornige stekelbaars” – or "tenspine stickleback". Based on my own counts, this is a more appropriate name.

One or two species of stickleback? Each student has to pass the test.

Here are our most important findings and some reflections:

1) Phenotypic divergence was significant for 50 % of homologous traits in threespine stickleback vs only 7 % in ninespine stickleback, while the proportion of outlier loci (SNPs which are likely genomic targets of selection) was at least 2.5 times larger in threespine stickleback. This confirms a stronger tendency to adapt in threespine stickleback. Since this is the first time that both species have been compared in exactly the same environmental matrix, we now know the effect of species-level differences in evolutionary versatility on population divergence.

2) These results do not imply that ninespine stickleback cannot adapt, since populations might already be preadapted to the environmental gradients in the study area. However, we observed a numerical advantage of the threespine stickleback in freshwater. We proposed that this relative ecological success could possibly be attributed to their evolutionary versatility. Of course, two species only represents a very small community, but it shows the potential of merging landscape genomics with community ecology to understand whether or not species evolve “collectively” across landscapes.

3) We observed substantial phenotypic, but no genomic parallelism between both species. This result demonstrates that the evolution of similar phenotypes in the same selective environments might primarily involve different genes. Based on previous comparative genomic studies, this result is not unexpected, but it is exciting to observe this in exactly the same spatial matrix. 

4) Note that we wanted our study to allow for a “fair” comparison of evolutionary versatility between the two species. We therefore compared both species for homologous traits only. Indeed, even if one species would be extremely variable for a trait which is missing in the other species, it would be hard to decide which species is most versatile. Luckily, most measurable traits in both species are homologous anyway (lateral plates, first dorsal spine, pelvic spine, gill rakers, fins, …). Non-homologous traits include dorsal spine #4, #5, #6, … #10 (guess which stickleback species is lacking those spines).

5) A reference genome is often used to facilitate SNP-typing. Yet, at present a reference genome is available for threespine stickleback, but not for ninespine stickleback. While it is possible to use the threespine stickleback genome as a reference for ninespine stickleback, we didn’t do this since this would narrow down the comparison between the two species to homologous genomic regions. Homologous traits do not necessarily have the same genetic basis, and hence the entire genome should be considered to allow for a straightforward comparison of evolutionary versatility. In addition, homologous genomic regions may already have gone through a long history of selection - perhaps pre-dating the origin of both species, and hence may bias our analyses in unexpected ways. In this respect our choice for de novo SNP typing in ninespine stickleback seemed more "safe". It is waiting now for the assembly of the ninespine stickleback genome to look into homology effects in detail.

The results are further discussed with respect to how differences in genomic architecture, gene flow and life history may induce or reflect variability in evolutionary potential and ecological success among species sharing the same landscape. Read more here.

Joost

Cited literature

Oke KB, Rolshausen G, LeBlond C, Hendry AP. 2017. How parallel is parallel evolution? A comparative analysis in fishes. The American Naturalist 190:1-16.

Raeymaekers JAM, Chaturvedi A, Hablützel PI, Verdonck I, Hellemans B, Maes GE, De Meester L, Volckaert FAM. 2017. Adaptive and non-adaptive divergence in a common landscape. Nature Communications.

Raeymaekers JAM, Konijnendijk N, Larmuseau MHD, Hellemans B, De Meester L, Volckaert FAM. 2014. A gene with major phenotypic effects as a target for selection vs. homogenizing gene flow. Molecular Ecology 23:162-181.

Stuart YE, Veen T, Weber JN, Hanson D, Ravinet M, Lohman BK, Thompson CJ, Tasneem T, Doggett A, Izen R, et al. 2017. Contrasting effects of environment and genetics generate a continuum of parallel evolution. 1:0158.