Multiple loci linked to inversions are associated with eye size variation in species of the Drosophila virilis phylad.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
30 07 2020
30 07 2020
Historique:
received:
24
04
2020
accepted:
14
07
2020
entrez:
1
8
2020
pubmed:
1
8
2020
medline:
10
2
2021
Statut:
epublish
Résumé
The size and shape of organs is tightly controlled to achieve optimal function. Natural morphological variations often represent functional adaptations to an ever-changing environment. For instance, variation in head morphology is pervasive in insects and the underlying molecular basis is starting to be revealed in the Drosophila genus for species of the melanogaster group. However, it remains unclear whether similar diversifications are governed by similar or different molecular mechanisms over longer timescales. To address this issue, we used species of the virilis phylad because they have been diverging from D. melanogaster for at least 40 million years. Our comprehensive morphological survey revealed remarkable differences in eye size and head shape among these species with D. novamexicana having the smallest eyes and southern D. americana populations having the largest eyes. We show that the genetic architecture underlying eye size variation is complex with multiple associated genetic variants located on most chromosomes. Our genome wide association study (GWAS) strongly suggests that some of the putative causative variants are associated with the presence of inversions. Indeed, northern populations of D. americana share derived inversions with D. novamexicana and they show smaller eyes compared to southern ones. Intriguingly, we observed a significant enrichment of genes involved in eye development on the 4th chromosome after intersecting chromosomal regions associated with phenotypic differences with those showing high differentiation among D. americana populations. We propose that variants associated with chromosomal inversions contribute to both intra- and interspecific variation in eye size among species of the virilis phylad.
Identifiants
pubmed: 32732947
doi: 10.1038/s41598-020-69719-z
pii: 10.1038/s41598-020-69719-z
pmc: PMC7393161
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
12832Références
Shapiro, M. D. et al. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717–723 (2004).
pubmed: 15085123
Sucena, É & Stern, D. L. Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. Proc. Natl. Acad. Sci. USA 97, 4530–4534 (2000).
pubmed: 10781057
Wittkopp, P. J., Williams, B. L., Selegue, J. E. & Carroll, S. B. Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes. Proc. Natl. Acad. Sci. USA. 100, 1808–1813 (2003).
pubmed: 12574518
Wittkopp, P. J. et al. Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in drosophila. Science 326, 540–544 (2009).
pubmed: 19900891
Hoekstra, H. E. Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97, 222–234 (2006).
pubmed: 16823403
Keesey, I. W. et al. Inverse resource allocation between vision and olfaction across the genus Drosophila. Nat. Commun. 10, 1–16 (2019).
Ramaekers, A. et al. Altering the temporal regulation of one transcription factor drives evolutionary trade-offs between head sensory organs. Dev. Cell 50, 780–792 (2019).
pubmed: 31447264
Stieb, S. M., Kelber, C., Wehner, R. & Rössler, W. Antennal-lobe organization in desert ants of the genus cataglyphis. Brain. Behav. Evol. 77, 136–146 (2011).
pubmed: 21502750
Sheehan, Z. B. V., Kamhi, J. F., Seid, M. A. & Narendra, A. Differential investment in brain regions for a diurnal and nocturnal lifestyle in Australian Myrmecia ants. J. Comp. Neurol. 527, 1261–1277 (2019).
pubmed: 30592041
Balkenius, A., Rosén, W. & Kelber, A. The relative importance of olfaction and vision in a diurnal and a nocturnal hawkmoth. J. Comp. Physiol. A 192, 431–437 (2006).
Montgomery, S. H. & Ott, S. R. Brain composition in Godyris zavaleta, a diurnal butterfly, reflects an increased reliance on olfactory information. J. Comp. Neurol. 523, 869–891 (2015).
pubmed: 25400217
Özer, I. & Carle, T. Back to the light, coevolution between vision and olfaction in the “dark-flies” (Drosophila melanogaster). PLoS ONE 15, e0228939 (2020).
pubmed: 32045466
pmcid: 7012446
Posnien, N. et al. Evolution of eye morphology and Rhodopsin expression in the Drosophila melanogaster species subgroup. PLoS ONE 7, e37346 (2012).
pubmed: 22662147
pmcid: 3360684
Gaspar, P. et al. Characterization of the genetic architecture underlying eye size variation within drosophila melanogaster and Drosophila simulans. G3 10, 1005–1018 (2020).
pubmed: 31919111
Norry, F. M., Vilardi, J. C. & Hasson, E. Negative genetic correlation between traits of the Drosophila head, and interspecific divergence in head shape. Heredity 85, 221–230 (2000).
Hämmerle, B. & Ferrús, A. Expression of enhancers is altered in Drosophila melanogaster hybrids. Evol. Dev. 5, 221–230 (2003).
pubmed: 12752761
Arif, S. et al. Genetic and developmental analysis of differences in eye and face morphology between Drosophila simulans and Drosophila mauritiana. Evol. Dev. 15, 257–267 (2013).
pubmed: 23809700
pmcid: 3799016
Hilbrant, M. et al. Sexual dimorphism and natural variation within and among species in the Drosophila retinal mosaic. BMC Evol. Biol. 14, 240. https://doi.org/10.1186/s12862-014-0240-x (2014).
doi: 10.1186/s12862-014-0240-x
pubmed: 25424626
pmcid: 4268811
Norry, F. M. & Gomez, F. H. Quantitative trait loci and antagonistic associations for two developmentally related traits in the drosophila head. J. Insect Sci. 17, 19 (2017).
pubmed: 28130460
pmcid: 5270402
Kirkpatrick, M. & Barton, N. Chromosome inversions, local adaptation and speciation. Genetics 173, 419–434 (2006).
pubmed: 16204214
pmcid: 1461441
Kirkpatrick, M. How and why chromosome inversions evolve. PLoS Biol. 8, e1000501 (2010).
pubmed: 20927412
pmcid: 2946949
Huang, W. et al. Natural variation in genome architecture among 205 Drosophila melanogaster genetic reference panel lines. Genome Res. 24, 1193–1208 (2014).
pubmed: 24714809
pmcid: 4079974
Durmaz, E., Benson, C., Kapun, M., Schmidt, P. & Flatt, T. An inversion supergene in Drosophila underpins latitudinal clines in survival traits. J. Evol. Biol. 31, 1354–1364 (2018).
pubmed: 29904977
pmcid: 6179442
Kapun, M. & Flatt, T. The adaptive significance of chromosomal inversion polymorphisms in Drosophila melanogaster. Mol. Ecol. 28, 1263–1282 (2019).
pubmed: 30230076
Fuller, Z. L., Koury, S. A., Phadnis, N. & Schaeffer, S. W. How chromosomal rearrangements shape adaptation and speciation: case studies in Drosophila pseudoobscura and its sibling species Drosophila persimilis. Mol. Ecol. 28, 1283–1301 (2019).
pubmed: 30402909
Norry, F. M., Vilardi, J. C., Fanara, J. J., Hasson, E. & Rodriguez, C. An adaptive chromosomal polymorphism affecting size-related traits, and longevity selection in a natural population of Drosophila buzzatii. Genetica 96, 285–291 (1995).
pubmed: 8522167
Fernández Iriarte, P. J., Norry, F. M. & Hasson, E. R. Chromosomal inversions effect body size and shape in different breeding resources in Drosophila buzzatii. Heredity 91, 51–59 (2003).
pubmed: 12815453
Hatadani, L. M. & Klaczko, L. B. Shape and size variation on the wing of Drosophila mediopunctata: influence of chromosome inversions and genotype-environment interaction. Genetica 133, 335–342 (2008).
pubmed: 17952608
Rako, L., Anderson, A. R., Sgrò, C. M., Stocker, A. J. & Hoffmann, A. A. The association between inversion In(3R)Payne and clinally varying traits in Drosophila melanogaster. Genetica 128, 373–384 (2006).
pubmed: 17028965
Wellenreuther, M. & Bernatchez, L. Eco-evolutionary genomics of chromosomal inversions. Trends Ecol. Evol. 33, 427–440 (2018).
pubmed: 29731154
Morales-Hojas, R. & Vieira, J. Phylogenetic patterns of geographical and ecological diversification in the subgenus Drosophila. PLoS ONE 7, e49552 (2012).
pubmed: 23152919
pmcid: 3495880
Russo, C. A. M., Mello, B., Frazão, A. & Voloch, C. M. Phylogenetic analysis and a time tree for a large drosophilid data set (Diptera: Drosophilidae). Zool. J. Linn. Soc. 169, 765–775 (2013).
Wittkopp, P. J. et al. Local adaptation for body color in Drosophila americana. Heredity 106, 592–602 (2011).
pubmed: 20606690
Reis, M. et al. A comparative study of the short term cold resistance response in distantly related Drosophila species: the role of regucalcin and Frost. PLoS ONE 6, e25520 (2011).
pubmed: 21991316
pmcid: 3184994
Fonseca, N. A. et al. Drosophila americana as a model species for comparative studies on the molecular basis of phenotypic variation. Genome Biol. Evol. 5, 661–679 (2013).
pubmed: 23493635
pmcid: 3641629
Reis, M. et al. Genes belonging to the insulin and ecdysone signaling pathways can contribute to developmental time, lifespan and abdominal size variation in Drosophila americana. PLoS ONE 9, e86690 (2014).
pubmed: 24489769
pmcid: 3904916
Throckmorton, L. H. The virilis species group. In The Genetics and Biology of Drosophila 3rd edn (eds Ashburner, M. & Novistky, E.) (Academic, New York, 1982).
Patterson, J. T. & Stone, W. S. The relationship of novamexicana to the other members of the virilis group. Univ. Texas Publ. 4920, 331–337 (1949).
Morales-Hojas, R., Vieira, C. P. & Vieira, J. Inferring the evolutionary history of Drosophila americana and Drosophila novamexicana using a multilocus approach and the influence of chromosomal rearrangements in single gene analyses. Mol. Ecol. 17, 2910–2926 (2008).
pubmed: 18482259
Hsu, T. C. Chromosomal variation and evolution in the virilis group of Drosophila. Univ. Texas Publ. 5204, 443–456 (1952).
Reis, M., Vieira, C. P., Lata, R., Posnien, N. & Vieira, J. Origin and consequences of chromosomal inversions in the virilis group of Drosophila. Genome Biol. Evol. 10, 3152–3166 (2018).
pubmed: 30376068
pmcid: 6278893
Haynie, J. L. & Bryant, P. J. Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster. J. Exp. Zool. 237, 293–308 (1986).
pubmed: 3084703
Treisman, J. E. Retinal differentiation in Drosophila. Wiley Interdiscip. Rev. Dev. Biol. 2, 545–557 (2013).
pubmed: 24014422
Şahin, H. B. & Çelik, A. Drosophila eye development and photoreceptor specification. eLS 23, 82–96 (2013).
Singh, J. & Mlodzik, M. Hibris, a Drosophila nephrin homolog, is required for presenilin-mediated notch and APP-like cleavages. Dev. Cell 23, 82–96 (2012).
pubmed: 22814602
pmcid: 3475182
Powell, P. A., Wesley, C., Spencer, S. & Cagan, R. L. Scabrous complexes with Notch to mediate boundary formation. Nature 409, 626–630 (2001).
pubmed: 11214322
Luque, C. M. & Milán, M. Growth control in the proliferative region of the Drosophila eye–head primordium: The elbow–noc gene complex. Dev. Biol. 301, 327–339 (2007).
pubmed: 17014842
Doroquez, D. B., Orr-Weaver, T. L. & Rebay, I. Split ends antagonizes the Notch and potentiates the EGFR signaling pathways during Drosophila eye development. Mech. Dev. 124, 792–806 (2007).
pubmed: 17588724
pmcid: 2231642
Rawlins, L. E. L., Lovegrove, B. & Jarman, A. P. Echinoid facilitates Notch pathway signalling during Drosophila neurogenesis through functional interaction with Delta. Development 130, 6475–6484 (2003).
pubmed: 14627723
Lu, X. & Li, Y. Drosophila Src42A is a negative regulator of RTK signaling. Dev. Biol. 208, 233–243 (1999).
pubmed: 10075855
Bai, J. M. et al. The cell adhesion molecule echinoid defines a new pathway that antagonizes the Drosophila EGF receptor signaling pathway. Development 128, 591–601 (2001).
pubmed: 11171342
Datta, R. R., Lurye, J. M. & Kumar, J. P. Restriction of ectopic eye formation by Drosophila teashirt and tiptop to the developing antenna. Dev. Dyn. 238, 2202–2210 (2009).
pubmed: 19347955
pmcid: 2733933
Jasper, H. et al. A genomic switch at the transition from cell proliferation to terminal differentiation in the Drosophila eye. Dev. Cell 3, 511–521 (2002).
pubmed: 12408803
Clusella-Trullas, S. & Terblanche, J. S. Local adaptation for body color in Drosophila americana: commentary on Wittkopp et al. Heredity 106, 904–905 (2011).
pubmed: 21063435
Reis, M., Valer, F. B., Vieira, C. P. & Vieira, J. Drosophila americana diapausing females show features typical of young flies. PLoS ONE 10, 671–675 (2015).
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH image to imageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
pubmed: 22930834
pmcid: 22930834
Rohlf, F. J. The tps series of software. Hystrix 26, 1 (2015).
Klingenberg, C. P. MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Resour. 11, 353–357 (2011).
pubmed: 21429143
Klingenberg, C. P. & Monteiro, L. R. Distances and directions in multidimensional shape spaces: implications for morphometric applications. Syst. Biol. 54, 678–688 (2005).
pubmed: 16126663
Claude, J. Morphometrics with R. (Springer, 2008).
Evans, A. L., Mena, P. A. & McAllister, B. F. Positive selection near an inversion breakpoint on the neo-X chromosome of Drosophila ameticana. Genetics 177, 1303–1319 (2007).
pubmed: 17660565
pmcid: 2147947
Fonseca, N. A., Vieira, C. P., Schlötterer, C. & Vieira, J. The DAIBAM MITE element is involved in the origin of one fixed and two polymorphic Drosophila virilis phylad inversions. Fly. 6, 71–74 (2012).
pubmed: 22561870
Clark, A. G. et al. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450, 203 (2007).
pubmed: 17994087
Pitnick, S., Markow, T. A. & Spicer, G. S. Delayed male maturity is a cost of producing large sperm in Drosophila. Proc. Natl. Acad. Sci. USA 92, 10614–10618 (1995).
pubmed: 7479851
Huxley, J. S. Constant differential growth-ratios and their significance. Nature 114, 895–896 (1924).
Huxley, J. S. & Teissier, G. Terminology of relative growth. Nature 137, 1–10 (1936).
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357 (2012).
pubmed: 22388286
pmcid: 3322381
Van der Auwera, G. A. et al. From fastQ data to high-confidence variant calls: the genome analysis toolkit best practices pipeline. Curr. Protoc. Bioinform. 43(1), 10–11 (2013).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168
pmcid: 19451168
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
López-Fernández, H. et al. bioinformatics protocols for quickly obtaining large-scale data sets for phylogenetic inferences. Interdiscip. Sci. Comput. Life Sci. 11, 1–9 (2019).
Vázquez, N. et al. BDBM 1.0: a desktop application for efficient retrieval and processing of high-quality sequence data and application to the identification of the putative coffea s-locus. Interdiscip. Sci. Comput. Life Sci. 11, 57–67 (2019).
Salmela, L. & Schroder, J. Correcting errors in short reads by multiple alignments. Bioinformatics 27, 1455–1461 (2011).
pubmed: 21471014
Jackman, S. D. et al. ABySS 2.0: resource-efficient assembly of large genomes using a Bloom filter. Genome Res. 27, 768–777 (2017).
pubmed: 28232478
pmcid: 5411771
Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
pubmed: 21988835
pmcid: 3261699
Glez-Peña, D., Gómez-Blanco, D., Reboiro-Jato, M., Fdez-Riverola, F. & Posada, D. ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Res. 38, W14–W18 (2010).
pubmed: 20439312
pmcid: 2896128
Ronquist, F. et al. Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
pubmed: 22357727
pmcid: 3329765
Maddison, W. P. Squared-change parsimony reconstructions of ancestral states for continuous-valued characters on a phylogenetic tree. Syst. Zool. 40, 304–314 (1991).
Rissman, A. I. et al. Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics 25, 2071–2073 (2009).
pubmed: 19515959
pmcid: 2723005
Wang, K., Li, M. & Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164 (2010).
pubmed: 20601685
pmcid: 2938201
Koestler, S. A., Alaybeyoglu, B., Weichenberger, C. X. & Celik, A. FlyOde: a platform for community curation and interactive visualization of dynamic gene regulatory networks in Drosophila eye development. F1000 Res. 4, 1484 (2015).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2018).
Fox, J. & Bouchet-Valat, M. Rcmdr: R Commander. (2018).
Fox, J. The R commander: a basic statistics graphical user interface to R. J. Stat. Softw. 14, 1–42 (2005).
Fox, J. Using the R Commander: A Point-and-Click Interface for R (Chapman and Hall/CRC Press, Boca Raton, 2017).
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, New York, 2016).