The roles of recombination and selection in shaping genomic divergence in an incipient ecological species complex

Wersebe, Matthew; Sherman, Ryan E.; Jeyasingh, Punidan D.; Weider, Lawrence J.

doi:10.1111/mec.16383

Cited by 11 publications

(18 citation statements)

References 178 publications

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“…First, these genes may be related to ongoing evolution of D. pulicaria during its recent invasion into lake ecosystems. Studies of the comparative genomics of D. pulicaria and its ecological-sister species D. pulex have noted that the differing growth and development phenotypes in these two species is underlain by distinct changes in developmental genes (57, 58). Thus, we may be picking up a global signal of adaptation in our study.…”

Section: Discussionmentioning

confidence: 99%

“…Increased salinity tolerance may require the accommodation of new developmental trajectories through phenotypic plasticity. Evolution via plasticity (59) requires that central developmental pathways serve as fuel for phenotypic differentiation (60). Furthermore, plasticity is thought to play an important role in rapid adaptation in Daphnia , a pattern we observe in the TL population (61–63).…”

Section: Discussionmentioning

confidence: 99%

“…Evolution via plasticity (59) requires that central developmental pathways serve as fuel for phenotypic differentiation (60). Furthermore, plasticity is thought to play an important role in rapid adaptation in Daphnia, a pattern we observe in the TL population (61)(62)(63). Regardless, testing of this assertion would be difficult because unlike other model arthropods, Daphnia development is not as well explored.…”

Section: Outliers and The Identification Of Candidate Genesmentioning

confidence: 93%

“…Thus, for this method we used only the samples collected from the water column in 2019. We ran six independent runs of this method using random subsets of 600,000 SNPs called in the population and a constant recombination rate of 7.2 cm/mb estimated from the D. pulicaria genetic map (57). In addition to LD-based methods, we estimated demographic parameters of the TL population - estimating N e and the population growth rate - by fitting a demographic model to the folded site frequency spectrum (SFS) implemented in FastSimcoal 2.7 (FSC2.7) (38).…”

Section: Methodsmentioning

confidence: 99%

“…Thus, f or this method we used only the samples collected f rom the water column in 2019. We ran six independent runs of this method using random subsets of 600,000 SNPs f rom all the SNPs called in the population and a constant recombination rate of 7.2 cm/mb estimated f rom the D. pulicaria genetic map (60). This analysis does not take in a given model a priori, instead it produces a population size trajectory that when inspected graphically can hint at dif ferent events (e.g., bottlenecks).…”

Section: Estimation Of Effective Population Size and Simulationsmentioning

confidence: 99%

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Resurrection genomics provides molecular and phenotypic evidence of rapid adaptation to salinization in a keystone aquatic species

Wersebe

Weider

2022

Preprint

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Ecologists and evolutionary biologists are increasingly cognizant of rapid adaptation in wild populations. Rapid adaptation to anthropogenic environmental change is critical for maintaining biodiversity and ecosystems services into the future. Anthropogenic salinization of freshwater ecosystems is quickly emerging as a primary threat, which is well documented in the northern temperate ecoregion. Specifically, many northern temperate lakes have undergone extensive salinization because of urbanization, including increased impervious surfaces for runoff, and the extensive use of road deicing salts (e.g., NaCl). It remains unclear if increasing salinization will lead to extirpation of species from these systems. Using a "resurrection genomics" approach, we investigated whether the keystone aquatic herbivore, Daphnia pulicaria, has evolved increased salinity tolerance in a severely salinized lake located in Minnesota, USA. Whole genome resequencing of 54 Daphnia clones hatched from resting eggs that represent a 25-year temporal contrast demonstrates that many regions of the genome containing genes related to osmoregulation are under selection in the study population. Tolerance assays of clones revealed that the most recent clones are more tolerant to salinity than older clones; this pattern is concomitant with the temporal pattern of increasing salinity in this lake. Together, our results demonstrate that keystone species such as Daphnia can rapidly adapt to increasing freshwater salinization. Further, our results indicate that rapid adaptation to salinity may allow lake Daphnia populations to persist in the face of anthropogenic salinization maintaining the food webs and ecosystem services they support despite global environmental change.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Outliers and The Identification Of Candidate Genesmentioning

confidence: 93%

Section: Methodsmentioning

confidence: 99%

Section: Estimation Of Effective Population Size and Simulationsmentioning

confidence: 99%

See 3 more Smart Citations

Resurrection genomics provides molecular and phenotypic evidence of rapid adaptation to salinization in a keystone aquatic species

Wersebe

Weider

2022

Preprint

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Resurrection genomics provides molecular and phenotypic evidence of rapid adaptation to salinization in a keystone aquatic species

Wersebe

Weider

2023

Proc. Natl. Acad. Sci. U.S.A.

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Ecologists and evolutionary biologists are increasingly cognizant of rapid adaptation in wild populations. Rapid adaptation to anthropogenic environmental change is critical for maintaining biodiversity and ecosystems services into the future. Anthropogenic salinization of freshwater ecosystems is quickly emerging as a primary threat, which is well documented in the northern temperate ecoregion. Specifically, many northern temperate lakes have undergone extensive salinization because of urbanization and the associated increase in impervious surfaces causing runoff, and the extensive use of road deicing salts (e.g., NaCl). It remains unclear whether increasing salinization will lead to extirpation of species from these systems. Using a “resurrection genomics” approach, we investigated whether the keystone aquatic herbivore, Daphnia pulicaria, has evolved increased salinity tolerance in a severely salinized lake located in Minnesota, USA. Whole-genome resequencing of 54 Daphnia clones from the lake and hatched from resting eggs that represent a 25-y temporal contrast demonstrates that many regions of the genome containing genes related to osmoregulation are under selection in the study population. Tolerance assays of clones revealed that the most recent clones are more tolerant to salinity than older clones; this pattern is concomitant with the temporal pattern of stabilizing salinity in this lake. Together, our results demonstrate that keystone species such as Daphnia can rapidly adapt to increasing freshwater salinization. Further, our results indicate that rapid adaptation to salinity may allow lake Daphnia populations to persist in the face of anthropogenic salinization maintaining the food webs and ecosystem services they support despite global environmental change.

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No recombination suppression in asexually produced males of Daphnia pulex

2023

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Obligate parthenogenesis (OP) is often thought to evolve by disruption of reductional meiosis and suppression of crossover recombination. In the crustacean Daphnia pulex, OP lineages, which have evolved from cyclical parthenogenetic (CP) ancestors, occasionally produce males that are capable of reductional meiosis. Here, by constructing high-density linkage maps, we find that these males show only slightly and non-significantly reduced recombination rates compared to CP males and females. Both meiosis disruption and recombination suppression are therefore sex-limited (or partly so), which speaks against the evolution of OP by disruption of a gene that is essential for meiosis or recombination in both sexes. The findings may be explained by female-limited action of genes that suppress recombination, but previously identified candidate genes are known to be expressed in both sexes. Alternatively, and equally consistent with the data, OP might have evolved through a re-use of the parthenogenesis pathways already present in CP and through their extension to all events of oogenesis. The causal mutations for the CP to OP transition may therefore include mutations in genes involved in oogenesis regulation and may not necessarily be restricted to genes of the “meiosis toolkit”. More generally, our study emphasizes that there are many ways to achieve asexuality, and elucidating the possible mechanisms is key to ultimately identify the genes and traits involved.

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The roles of recombination and selection in shaping genomic divergence in an incipient ecological species complex

Cited by 11 publications

References 178 publications

Resurrection genomics provides molecular and phenotypic evidence of rapid adaptation to salinization in a keystone aquatic species

Resurrection genomics provides molecular and phenotypic evidence of rapid adaptation to salinization in a keystone aquatic species

Resurrection genomics provides molecular and phenotypic evidence of rapid adaptation to salinization in a keystone aquatic species

No recombination suppression in asexually produced males of Daphnia pulex

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