A possible genomic footprint of polygenic adaptation on population divergence in seed beetles?
Abstract Efforts to unravel the genomic basis of incipient speciation are hampered by a mismatch between our toolkit and our understanding of the ecology and genetics of adaptation. While the former is focused on detecting selective sweeps involving few independently acting or linked speciation gene...
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| Format: | Article |
| Language: | English |
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Wiley
2022-10-01
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| Series: | Ecology and Evolution |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/ece3.9440 |
| _version_ | 1811213131200856064 |
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| author | Göran Arnqvist Ahmed Sayadi |
| author_facet | Göran Arnqvist Ahmed Sayadi |
| author_sort | Göran Arnqvist |
| collection | DOAJ |
| description | Abstract Efforts to unravel the genomic basis of incipient speciation are hampered by a mismatch between our toolkit and our understanding of the ecology and genetics of adaptation. While the former is focused on detecting selective sweeps involving few independently acting or linked speciation genes, the latter states that divergence typically occurs in polygenic traits under stabilizing selection. Here, we ask whether a role of stabilizing selection on polygenic traits in population divergence may be unveiled by using a phenotypically informed integrative approach, based on genome‐wide variation segregating in divergent populations. We compare three divergent populations of seed beetles (Callosobruchus maculatus) where previous work has demonstrated a prominent role for stabilizing selection on, and population divergence in, key life history traits that reflect rate‐dependent metabolic processes. We derive and assess predictions regarding the expected pattern of covariation between genetic variation segregating within populations and genetic differentiation between populations. Population differentiation was considerable (mean FST = 0.23–0.26) and was primarily built by genes showing high selective constraints and an imbalance in inferred selection in different populations (positive Tajima's DNS in one and negative in one), and this set of genes was enriched with genes with a metabolic function. Repeatability of relative population differentiation was low at the level of individual genes but higher at the level of broad functional classes, again spotlighting metabolic genes. Absolute differentiation (dXY) showed a very different general pattern at this scale of divergence, more consistent with an important role for genetic drift. Although our exploration is consistent with stabilizing selection on polygenic metabolic phenotypes as an important engine of genome‐wide relative population divergence and incipient speciation in our study system, we note that it is exceedingly difficult to firmly exclude other scenarios. |
| first_indexed | 2024-04-12T05:40:36Z |
| format | Article |
| id | doaj.art-0e68faf5d7c3446bab07b35e75eb9a8b |
| institution | Directory Open Access Journal |
| issn | 2045-7758 |
| language | English |
| last_indexed | 2024-04-12T05:40:36Z |
| publishDate | 2022-10-01 |
| publisher | Wiley |
| record_format | Article |
| series | Ecology and Evolution |
| spelling | doaj.art-0e68faf5d7c3446bab07b35e75eb9a8b2022-12-22T03:45:39ZengWileyEcology and Evolution2045-77582022-10-011210n/an/a10.1002/ece3.9440A possible genomic footprint of polygenic adaptation on population divergence in seed beetles?Göran Arnqvist0Ahmed Sayadi1Animal Ecology, Department of Ecology and Genetics, EBC Uppsala University Uppsala SwedenAnimal Ecology, Department of Ecology and Genetics, EBC Uppsala University Uppsala SwedenAbstract Efforts to unravel the genomic basis of incipient speciation are hampered by a mismatch between our toolkit and our understanding of the ecology and genetics of adaptation. While the former is focused on detecting selective sweeps involving few independently acting or linked speciation genes, the latter states that divergence typically occurs in polygenic traits under stabilizing selection. Here, we ask whether a role of stabilizing selection on polygenic traits in population divergence may be unveiled by using a phenotypically informed integrative approach, based on genome‐wide variation segregating in divergent populations. We compare three divergent populations of seed beetles (Callosobruchus maculatus) where previous work has demonstrated a prominent role for stabilizing selection on, and population divergence in, key life history traits that reflect rate‐dependent metabolic processes. We derive and assess predictions regarding the expected pattern of covariation between genetic variation segregating within populations and genetic differentiation between populations. Population differentiation was considerable (mean FST = 0.23–0.26) and was primarily built by genes showing high selective constraints and an imbalance in inferred selection in different populations (positive Tajima's DNS in one and negative in one), and this set of genes was enriched with genes with a metabolic function. Repeatability of relative population differentiation was low at the level of individual genes but higher at the level of broad functional classes, again spotlighting metabolic genes. Absolute differentiation (dXY) showed a very different general pattern at this scale of divergence, more consistent with an important role for genetic drift. Although our exploration is consistent with stabilizing selection on polygenic metabolic phenotypes as an important engine of genome‐wide relative population divergence and incipient speciation in our study system, we note that it is exceedingly difficult to firmly exclude other scenarios.https://doi.org/10.1002/ece3.9440accessory gland proteinsCallosobruchus maculatusepistasisincipient speciationmetabolic rateseminal fluid proteins |
| spellingShingle | Göran Arnqvist Ahmed Sayadi A possible genomic footprint of polygenic adaptation on population divergence in seed beetles? Ecology and Evolution accessory gland proteins Callosobruchus maculatus epistasis incipient speciation metabolic rate seminal fluid proteins |
| title | A possible genomic footprint of polygenic adaptation on population divergence in seed beetles? |
| title_full | A possible genomic footprint of polygenic adaptation on population divergence in seed beetles? |
| title_fullStr | A possible genomic footprint of polygenic adaptation on population divergence in seed beetles? |
| title_full_unstemmed | A possible genomic footprint of polygenic adaptation on population divergence in seed beetles? |
| title_short | A possible genomic footprint of polygenic adaptation on population divergence in seed beetles? |
| title_sort | possible genomic footprint of polygenic adaptation on population divergence in seed beetles |
| topic | accessory gland proteins Callosobruchus maculatus epistasis incipient speciation metabolic rate seminal fluid proteins |
| url | https://doi.org/10.1002/ece3.9440 |
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