DOI: 10.5061/dryad.63xsj3v6f
title: Candidate gene polymorphisms are linked to dispersive and migratory behaviour: searching for a mechanism behind the “paradox of the great speciators”

description: The “paradox of the great speciators” has puzzled evolutionary biologists
 for over half a century. A great speciator requires excellent dispersal
 propensity to explain its occurrence on multiple islands, but reduced
 dispersal ability to explain its high number of subspecies. A rapid
 reduction in dispersal ability is often invoked to solve this apparent
 paradox, but a proximate mechanism has not been identified yet. Here, we
 explored the role of six genes linked to migration and animal personality
 differences (CREB1, CLOCK, ADCYAP1, NPAS2, DRD4, and SERT) in 20 South
 Pacific populations of silvereye (Zosterops lateralis) that range from
 highly sedentary to partially migratory, to determine if genetic variation
 is associated with dispersal propensity and migration. We detected genetic
 associations in three of the six genes: i) in a partial migrant
 population, migrant individuals had longer microsatellite alleles at the
 CLOCK gene compared to resident individuals from the same population; ii)
 CREB1 displayed longer average microsatellite allele lengths in recently
 colonised island populations (&lt; 200 years), compared to
 evolutionarily older populations. Bayesian broken stick regression models
 supported a reduction in CREB1 length with time since colonisation; and
 iii) like CREB1, DRD4 showed differences in polymorphisms between recent
 and old colonisations but a larger sample is needed to confirm. ADCYAP1,
 SERT, and NPAS2 were variable but that variation was not associated with
 dispersal propensity. The association of genetic variants at three genes
 with migration and dispersal ability in silvereyes provides the impetus
 for further exploration of genetic mechanisms underlying dispersal shifts
 and the prospect of resolving a long-running evolutionary paradox through
 a genetic lens.
description: # Candidate gene polymorphisms are linked to dispersive and migratory
 behaviour: searching for a mechanism behind the “paradox of the great
 speciators” *** Estandía et al. 2023 is motivated by the concept of the
 “paradox of the great speciators”, that is those subspecies-rich birds
 distributed across multiple islands. The paradox lies in their wide
 distributions suggesting excellent dispersal ability, combined with, high
 subspecific diversity suggesting limits to dispersal. Could this paradox
 be resolved if there were genetic switches associated with dispersal? We
 examined if genetic variation at six genes linked to migration and animal
 personality differences was associated with variation in dispersal
 propensity in 422 individuals from 20 populations of silvereye
 (*Zosterops* *lateralis*) in Australia and the south-west Pacific. We
 found several genetic associations: in a partial migrant population,
 migrant individuals had longer microsatellite alleles at the *CLOCK* gene
 compared to residents; *CREB1* displayed longer average microsatellite
 allele lengths in recently colonised island populations (&lt; 200
 years), compared to evolutionarily older populations and furthermore,
 modelling supported a reduction in *CREB1* length with time since
 colonisation and decreasing dispersal propensity, potentially indicating
 selection against dispersal following island colonisation. Results from
 other genes were equivocal or showed no association with dispersal
 propensity. Nevertheless our results show that the paradox can be partly
 understood through a genetic lens. ## Description of the data and file
 structure # Dryad **INPUT DATA** 1. `curated_dataset`: main curated
 dataset: 1. Order: order of the samples sorted alphabetically by
 population 2. common\_name: common name for the species 3. species:
 scientific name for the species 4. subspecies: scientific name for the
 subspecies 5. country: country where the sample was collected 6. state:
 state, if relevant, where the sample was collected 7. population:
 population defined as island if no genetic substructure 8. island: only
 relevant for island populations 9. town\_region: region where the sample
 was collected (e.g. Canberra) 10. location: location where the sample was
 collected (e.g. Australian National Botanical Garden, in Canberra) 11.
 site: particular site within location where the sample was collected 12.
 migrant: migratory status as calculated in `1.0_model_migrants.Rmd`
 notebook at
 `https://github.com/andreaestandia/1.0_silvereye_candidate_genes` 13.
 name: field sample name, mostly the same as id expect for a few from
 Aotearoa New Zealand 14. id: blood id 15. measured\_by: fieldworker who
 took measurements of the bird 16. fieldtrip: which fieldtrip the sample
 was collected in 17. date 18. time 19. latitude 20. longitude 21.
 disp\_index: dispersal index as calculated by equation 1 available in
 materials and methods 22. age\_myr: age of the population in millions of
 years 23. isolation\_index: isolation index. distance between islands 24.
 area: area of the island 25. short\_adcyap: for microsatellite candidate
 genes there are often two peaks, `short_gene` represents the shorter one,
 `long_gene` the long one and `mean_gene` the average between short and
 long 26. long\_adcyap 27. mean\_adcyap 28. short\_creb1 29. long\_creb1
 30. mean\_creb1 31. short\_clock 32. long\_clock 33. mean\_clock 34.
 short\_npas2 35. long\_npas2 36. mean\_npas2 37. DRD4\_snp1218: each of
 these columns represent SNPs for *DRD4* and *SERT* . 0 and 1 represent
 each of the variants 38. DRD5\_snp1228 39. DRD6\_snp140 40. DRD7\_snp150
 41. DRD8\_snp217 42. DRD9\_snp224 43. DRD10\_snp41 44. DRD11\_snp742 45.
 DRD12\_snp83 46. DRD13\_snp926 47. SERT\_indel195 48. SERT\_snp266 49.
 SERT\_snp311 50. cluster: k1 represents the SM cluster and k2 the ANZO
 cluster 51. locator\_x: locators are used for the structure plots to get
 the right order of populations 52. locator 53. locator2 2.
 `202000224_Candidategenes.geneious`: it contains the raw and processed
 geneious files for candidate genes 3. `subset-genotype-phenotype-genpop`:
 input for genpop to estimate HWE and allelic richness 4.
 `aus_wholegenome_10K_* and mel_wholegenome_10K_*`: input files to estimate
 gene flow with BayesAss3-SNP
 ([https://github.com/stevemussmann/BayesAss3-SNPs](https://github.com/stevemussmann/BayesAss3-SNPs)) 5. `wholegenome_pruned_1million`\*: input files to estimate population structure with NGSAdmix ([http://www.popgen.dk/software/index.php/NgsAdmix](http://www.popgen.dk/software/index.php/NgsAdmix)) 1. wholegenome\_pruned\_1million\_melanesia\_subset.beagle.gz: samples from the SM cluster 2. wholegenome\_pruned\_1million\_subset\_oz.beagle.gz: samples for the ANZO cluster 3. wholegenome\_pruned\_1million\_subset.beagle.gz: all samples pooled together 6. `island_labels` and `islands_info`: they contain essential information to reproduce Figure 1 7. `pop_covariance_matrix`: population-level covariance matrix used to produce the heatmap in Figure S3 **OUTPUT DATA** 1. `pcangsd_output.cov`: raw output from PCAngsd 2. `migrants.cov`: raw output from PCAngsd for the migratory and resident Tasmanian samples 3. `*rds`: any file with RDS extension is the output of a model. Those models with the *\_long* word before the *rds* extension, represent the same models with using the longer allele. 1. `mcp_creb_age.rds`: Broken stick regression output for *CREB1* with population age as explanatory variable 2. `mcp_creb_age_null.rds`: Null model. Broken stick regression output for *CREB1* with population age as explanatory variable 3. `mcp_creb_disp.rds`: Broken stick regression output for *CREB1* with dispersal propensity as explanatory variable 4. `mcp_creb_disp_null.rds`: Null model. Broken stick regression output for *CREB1* with dispersal propensity as explanatory variable 5. `mod_clock_pop.rds`: Model output. Differences among populations at *CLOCK* 6. `mod_adcyap_pop.rds`: Model output. Differences among populations at *ADCYAP1* 7. `mod_npas_pop.rds`: Model output. Differences among populations at *NPAS2* 8. `mod_creb1_pop.rds`: Model output. Differences among populations at *CREB1* 9. `brms_creb_null.rds`: Null model. Generalised linear mixed model output for *CREB1* with pop age and dispersal propensity as explanatory variables 10. `brms_creb.rds`: Generalised linear mixed model output for *CREB1* with pop age and dispersal propensity as explanatory variables 11. `brms_adcyap_null.rds`: Null model. Generalised linear mixed model output for *ADCYAP1* with pop age and dispersal propensity as explanatory variables 12. `brms_adcyap.rds`: Generalised linear mixed model output for *ADCYAP1* with pop age and dispersal propensity as explanatory variables 13. `brms_clock_migratory.rds`: Model output. Differences between migratory and resident birds at *CLOCK* <br> ## Code/Software Code to reproduce all analyses can be found here: https://github.com/andreaestandia/1.0\_silvereye\_candidate\_genes