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Wing Geometry and Genetic Analyses Reveal Contrasting Spatial bioRxiv preprint doi: https://doi.org/10.1101/2020.09.16.299487; this version posted September 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Wing Geometry and Genetic Analyses Reveal Contrasting Spatial 2 Structures between Male and Female Aedes aegypti Populations in 3 Metropolitan Manila, Philippines 4 Thaddeus M. Carvajal1, 2, 3, Divina M. Amalin2, 3 and Kozo Watanabe1, 2,3a 5 6 1 Center for Marine Environmental Studies (CMES) - Ehime University, Matsuyama, Japan 7 8 2 Biological Control Research Unit, Center for Natural Science and Environmental 9 Research - De La Salle University, Taft Ave Manila, Philippines 10 11 3 Biology Department, College of Science - De La Salle University, Taft Ave Manila, 12 Philippines 13 14 a Corresponding author: [email protected] 15 Emails: 16 TMC: [email protected] 17 DMA: [email protected] 18 KW: [email protected] 19 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.16.299487; this version posted September 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 20 Abstract 21 Background Many important arboviral diseases (e.g. dengue, chikungunya) are transmitted 22 by the bite of a female mosquito vector, Aedes aegypti. Hence, the population genetic 23 structure of the mosquito has been studied in order to understand its role as an efficient 24 vector. Several studies utilized an integrative approach; to combine genetic and phenotypic 25 data to determine the population structure of Ae. aegypti but these studies have only 26 focused on female populations. To address this particular gap, our study compared the 27 population variability and structuring between male and female Ae. aegypti populations 28 using phenotypic (wing geometry) and genetic (microsatellites) data from a highly- 29 urbanized and dengue-endemic region of the Philippines, Metropolitan Manila. 30 Methods. Five mosquito populations comprised of female (n = 137) and male (n = 49) 31 adult Ae. aegypti mosquitoes were used in this study. All mosquito individuals underwent 32 geometric morphometric (26 landmarks), and genetic (11 microsatellite loci) analyses. 33 Results. Results revealed that FST estimates (genetic) were 0.055 and 0.009 while QST 34 estimates (phenotypic) were 0.318 and 0.309 in in male and female populations, 35 respectively. Wing shape variation plots showed that male populations were distinctly 36 separated from each other while female populations overlapped. Similarly, discriminant 37 analysis of principal components using genetic data revealed that male populations were 38 also distinctly separated from each other while female populations showed near- 39 overlapping populations. Genetic and phenetic dendrograms showed the formation of two 40 groups in male populations but no groups in female populations. Further analysis indicated 41 a significant correlation (r = 0.68, p = 0.02) between the genetic and phenetic distances of 42 male populations. Bayesian analysis using genetic data also detected multiple clusters in 43 male (K = 3) and female (K = 2) populations, while no clusters were detected using the 44 phenotypic data from both sexes. 45 Conclusions. Our results revealed contrasting phenotypic and genetic patterns between 46 male and female Ae. aegypti, indicating that male populations were more spatially bioRxiv preprint doi: https://doi.org/10.1101/2020.09.16.299487; this version posted September 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 47 structured than female populations. Although genetic markers demonstrated higher 48 sensitivity in detecting population structures than phenotypic markers, correlating patterns 49 of population structure were still observed between the two markers. 50 Keywords Dengue, Geometric Morphometrics, Microsatellites 51 52 Background 53 Aedes aegypti is the primary mosquito vector for several important mosquito-borne 54 diseases such as dengue, chikungunya and Zika. Over the past decade, many scientists have 55 focused on studying the population genetic structuring of this species within urban areas1-6. 56 Genetic markers such as microsatellite loci and single nucleotide polymorphisms (SNPs) 57 have been largely used to investigate the population structure of Ae. aegypti on macro- and 58 micro-geographic scales which revealed high genetic diversity and distinct genetic 59 clustering in different regions and countries7-9, cities and villages1,2,6. 60 Wing geometry is a phenotypic marker that can be used as an alternative approach 61 to describe the population variability and structure of Ae. aegypti since these are 62 evolutionarily informative and heritable10,11. Previous studies on Ae. aegypti have 63 demonstrated that wing shape can be an indicator of population genetic structure in fine- 64 scale areas12,13. It can also detect subtle variation within a single mosquito population either 65 over time (e.g. temporal variation)4 or along environmental gradients (e.g. altitude, levels of 66 urbanization) 14,15. For this reason, estimating the population genetic structure using wing 67 geometry has been supported by many studies because of its low-cost alternative10. 68 Many independent studies have focused on either genetic or phenotypic markers, 69 but some several studies have also integrated both markers16-19, especially in Ae. aegypti3,4. 70 Patterns of wing shape variation and genetic diversity in Ae. vexans indicated distinct 71 spatial structural differences from northern and central European countries with 72 considerable gene flow on a regional scale19. Parallel temporal changes in allelic 73 frequencies and wing shape were also observed in Ae. aegypti from Brazil, suggesting that bioRxiv preprint doi: https://doi.org/10.1101/2020.09.16.299487; this version posted September 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 74 these changes could be driven by genetic drift and divergent selection4, however, the results 75 generated by genetic and phenotypic markers have often contradicted each other. For 76 example, estimates of the morphological diversity index (QST) have often been larger than 3,4 77 the genetic diversity index (FST) from mosquito populations at the micro- and macro- 78 geographical16 scale in Brazil. Wing shape was also unable to show clear patterns of 79 population differentiation compared to genetic markers at these scales3,18. The slow 80 evolutionary rate of change for wing shape which has resulted in morphological uniformity 81 or homogeneity could be due to high gene flow or continuous migrations of this mosquito 82 vector that counteract local genetic drift10,20. More importantly, since wings of Ae. aegypti 83 are important organs for flight and sexual signaling, selective pressure may have stabilized 84 them over time21. 85 The majority of these integrative (wing geometry and genetic) analysis 86 investigations only focused on female Ae. aegypti populations. This may be due to the 87 importance of female mosquitoes in transmitting arboviruses, but research focusing on male 88 Ae. aegypti mosquitoes is becoming equally important due to its notable role in vector 89 control strategies, particularly in rear-release methods such as sterile insect technique (SIT), 90 insect incompatibility technique (IIT) and genetically modified mosquitoes (GMM)22-24. 91 Notable biological differences in male and female Ae. aegypti mosquitoes could affect 92 genetic and phenotypic variability as well as the spatial structuring of each sex. For 93 instance, smaller-sized male mosquitoes may have shorter dispersal distance, thereby 94 producing heterogeneous male populations even on the micro-geographic scale. This was 95 exemplified in our previous wing geometry study12 which revealed the fine-scale 96 population structure in male mosquitoes with short dispersal distances (up to 22 km). 97 The aim of this study was to describe and compare the population variability and 98 structure between male and female Ae. aegypti mosquitoes using wing geometry and 99 genetic markers. Adult Ae. aegypti mosquitoes were collected from within a highly- 100 urbanized and dengue-endemic region of the Philippines, Metropolitan Manila. Eleven 101 microsatellite loci and 26 identified morphometric landmarks were used to compare both bioRxiv preprint doi: https://doi.org/10.1101/2020.09.16.299487; this version posted September 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 102 sexes. Unlike previous studies that used different mosquito individuals for each approach3, 103 16-18, we utilized the same mosquito for genetic and morphometric analysis in order to 104 reflect and compare the population variability and structure for both markers. 105 Methods 106 Study Area and Mosquito Sampling 107 Collection of Ae. aegypti adult mosquitoes was conducted within Metropolitan 108 Manila, Philippines (Figure 1) from May 2014 to January 2015. Households were selected 109 based on voluntary consent to collecting adult mosquitoes on their premises. The collection 110 procedure, sorting, preservation and identification of adult mosquitoes was based on 111 Carvajal et al.6 while sex determination of each adult was performed using the 112 morphological pictorial keys from Rueda et al.
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