Connections between ploidy and environment in South American frogs

Polyploid frogs occur mainly in the SE corner of South America to the apparent exclusion of closely related diploids, a trend that persists across genera.

Above: Occurrences and range maps of all the frogs included in the study,
grouped by genus and colored by ploidy

Genome duplications are one of the most extreme mutations that can be found in nature. Lineages that undergo genome duplication (called polyploids) experience traumatic changes on the molecular and cellular level that are known to incur significant fitness costs. However, the increase of genetic material also provides the opportunity for adaptation. Polyploids experience more mutations per gene, allowing now-redundant gene copies to develop new functions. The various potential costs and benefits of genome duplication combine to create a unique evolutionary trajectory for polyploids. In particular, many polyploid species are known to inhabit new, challenging or disrupted environments that are subject to greater environmental extremes than experienced by their diploid counterparts. For example, polyploid species are often found in areas that have been recently glaciated and they also make up a large proportion of invasive plant species.

Editors’ Choice article: (Free to read online for a year.)
David, K.T. and Halanych, K.M. (2021), Spatial proximity between polyploids across South American frog genera. J Biogeogr. 48: xxx–xxx. 

Much of my PhD dissertation work focuses on the evolutionary consequences of gene and genome duplication on the molecular level, but while reading I started to become more interested in this relationship between environment and ploidy. I decided to focus my investigation on frogs, a group with lots of publicly available locality data, and restrict my search to South America which has a large number of polyploid frog species across multiple clades.

The preliminary results were striking. Not only were polyploid and diploid species ranges largely separate from one another, there seemed to be a recurring pattern across genera of polyploid lineages occurring in the southeast region of the continent. To us, this suggested a particular environment that was conducive to the formation and/or maintenance of polyploid species. This pattern was corroborated with range overlap analysis which indicated greater overlap between polyploid lineages than diploid lineages across the phylogeny. Indeed, on average polyploid species occur closer to other polyploids of different genera than they do to diploids of their own genus. To explore this idea further we collected all the information we could on the environmental and climatic conditions of the region. Polyploids seem to overwhelmingly prefer temperate climates (84.7% of occurrences) whereas the most popular climate for diploids was tropical (42.6%), which polyploids almost entirely avoid (6.6%). Similarly, polyploids have less than half the relative frequency in forested biomes (31.1%) than diploids (63.2%). Instead, polyploid occurrences are more common in grasslands, savannas and shrublands (58.7%). In addition to biome classifications, we also looked at whether or not any continuous environmental variables were significantly different between polyploid and diploid species. Using a phylogenetic ANOVA test, we found that temperature seasonality (standard deviation of temperature over the course of the year) was the only variable significantly different between polyploids and diploids. Temperature fluctuations have been linked to fish and amphibian polyploids before, possibly connected to their ability to resist environmental disruptions. However, changes in temperature could also result in an increase in polyploid formation, as temperature shocks are a well-documented method for inducing whole genome duplications in many aquaculture species, as well as frogs.

Heatmaps of temperature seasonality and cropland usage alongside occurrence and range maps of all frogs included in the study

Another difference between polyploid and diploid occurrences appears to be human impacts. Southeastern South America has experienced rapid agricultural development over the last century, resulting in one of the largest biodiversity declines in the world. As polyploids are thought to be more adaptable or resistant to challenging/disrupted environments its possible they are able to survive in this transformed landscape in ways diploids are not. In each of the sampled genera, polyploids were more frequent in areas with higher cropland usage, fertilizer application, and pesticide application compared to diploids between every comparison with statistical significance. Importantly, phylogenetic ANOVAs comparing these variables were not significant, meaning that we cannot discount the possibility that differences are the result of shared ancestry between occurrences rather than ploidy alone. As a result, we considered the human impact hypothesis to be a little more speculative than the temperature seasonality hypothesis, but still merits further investigation, as there does appear to be a strong correlation between ploidy and human impacts in at least some of the genera under study. We hope that our findings prove useful in understanding how polyploid lineages are formed and persist in nature, and lead to further investigations into the relationship between ploidy and environment.

Written by:
Kyle David

PhD candidate, Auburn University, USA

Additional information:
Twitter: @KyleTheDavid

Published by jbiogeography

Contributing to the growth and societal relevance of the discipline of biogeography through dissemination of biogeographical research.

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