Influence of Historical and Human Factors on Genetic

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Influence of Historical and Human Factors on Genetic bioRxiv preprint doi: https://doi.org/10.1101/2020.04.06.027219; this version posted April 7, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 Influence of historical and human factors on genetic structure and diversity 2 patterns in peripheral populations: implications for the conservation of Moroccan 3 trout 4 Perea S1*, Al Amouri M2, Gonzalez EG1, Alcaraz L1, Yahyaoui A2, Doadrio I1 5 1Biodiversity and Evolutionary Biology Department, Museo Nacional de Ciencias 6 Naturales, CSIC. Madrid, Spain. 7 2Laboratory of Biodiversity, Ecology and Genome, Faculty of Sciences, Mohammed V 8 University. Rabat. Rabat. Morocco. 9 *Correspondence: Silvia Perea. Biodiversity and Evolutionary Biology Department, 10 Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal, 2. 28006 Madrid. 11 Spain. E-mail: [email protected] 1 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.06.027219; this version posted April 7, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 12 Abstract 13 1.The brown trout s.l. has been the focus of numerous phylogeographic and conservation 14 studies due to its socioeconomic importance, its marked genetic and phenotypic 15 differentiation and its broad distribution range. Especially interesting evolutionary patterns are 16 observed for populations occupying peripheral areas of a distribution range, such as in the 17 case of the highly isolated trout populations in Morocco. 18 2.Continuous stocking programs may conceal natural genetic patterns, making it challenging 19 to discern evolutionary patterns. In Morocco, trout stocking programs have been implemented 20 to increase the genetic diversity of native populations by pooling fish of different origins in 21 the Ras el Ma hatchery (Azrou region) and then stocking them in the different basins. In this 22 study, phylogenetic and phylogeographic patterns, as well as genetic structure and diversity, 23 of Moroccan trout populations were analyzed to evaluate the impact of continuous fish 24 stocking on evolutionary processes in order to better distinguish between natural and human- 25 mediated patterns. 26 3.Two mitochondrial and nine microsatellite markers were analyzed for all populations along 27 the entire distribution range of brown trout in Morocco. Phylogenetic and phylogeographic 28 analyses rendered two highly divergent evolutionary lineages, one comprising populations in 29 the Drâa Basin and a second grouping the remaining Moroccan populations. Divergence of 30 the Drâa lineage occurred during the Upper Pliocene, whilst differentiation within the second 31 lineage coincided with the onset of the Pleistocene. 32 4.Genetic structuring among populations was evident. Nevertheless, populations exhibiting 33 higher levels of genetic diversity were those affected by human-mediated processes, making it 34 difficult to associate this diversity with natural processes. In fact, highly geographically 35 isolated, not stocked populations showed the lowest values of genetic diversity. Although 36 stocking management may increase the genetic diversity of these populations, it could also 37 lead to the loss of local adaptive genotypes. Hence, current trout conservation programs 38 should be revised. 39 Keywords: biodiversity, conservation evaluation, fish, genetics, rivers, streams 40 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.06.027219; this version posted April 7, 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. 41 1. Introduction 42 Biodiversity loss in freshwater systems is occurring at a faster rate than in terrestrial 43 environments (Dudgeon et al., 2006; Strayer & Dudgeon, 2010). Exploitation of water 44 resources, habitat alterations, mainly due to water extraction for agriculture, hydraulic 45 infrastructure construction and urban water use, along with the introduction of exotic species, 46 is exacerbating this loss of freshwater biodiversity (Dudgeon et al., 2006). In the 47 Mediterranean region, climate models predict an increase in temperature and a decrease in 48 precipitation that will decrease the availability of water resources and intensify the effects of 49 increasing human pressure upon freshwater ecosystems (García-Ruiz, López-Moreno, Vicente 50 Serraron, Lasanta-Martínez & Beguería, 2011; Guiot & Cramer, 2016). Populations located in 51 the periphery of the species distribution ranges would be especially vulnerable to these global 52 warming effects, especially in the southern periphery, that could increase the extinction risk of 53 these populations (Gibson, van der Marel & Starzomski, 2009). Within this context, 54 freshwater fish faunas are considered useful indicators of trends in aquatic ecosystems due to 55 their intrinsic characteristics such as being at the top of food webs or their long longevity and 56 high mobility (Li, Zheng & Liu, 2010; Estevez et al., 2017). Some groups are especially good 57 indicators of water quality due to their specific ecological and habitat requirements. For 58 example, salmonids (e.g. trout, salmon and char) have very restricted ecological requirements 59 such as cold, clean and well-oxygenated waters and, therefore, are highly sensitive to habitat 60 change (Almodovar, Nicola, Ayllon & Elvira, 2012; Merrian, Fernandez, Petty & Zegre, 61 2017; Young et al., 2018). 62 Within salmonids, the brown trout is distributed widely across Europe, North Africa 63 and western Asia. Morocco constitutes the southwestern limit of the brown trout distribution 64 range and suitable habitats for these organisms in this region are found at higher altitudes than 65 in the northern latitudes. Consequently, these southern peripheral Moroccan trout populations 66 have a fragmented distribution and are mainly located in headwaters of high-altitude rivers, in 67 most cases only in the sources of these rivers, and in oligotrophic lakes in the Atlas 68 Mountains. Some populations are also found at lower altitudes in the Mediterranean slope of 69 the Rifian region but only in areas characterized by steep slopes with fast currents and 70 oxygenated waters (Pellegrin, 1924). Peripheral populations of widely distributed species, as 71 Moroccan trout, are expected not only to be more geographically isolated, showing a strong 72 population structure but also to have smaller effective population sizes and lower genetic 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.06.027219; this version posted April 7, 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. 73 diversity (see Eckert, Samis & Lougheed, 2008 for a review of genetic diversity in peripheral 74 populations). For these reasons, knowing the genetic structure and diversity of Moroccan trout 75 populations is vital in order to evaluate the conservation status of these populations and to 76 design appropriate conservation strategies according to the needs and characteristics of 77 organisms from the peripheral areas of distribution ranges; Siler, Oaks, Cobb, Ota & Brown, 78 2014; Thorton et al., 2017). 79 For these conservation strategies, parameters such as genetic structure and diversity of 80 populations, or demographic trends, are critical to design accurate plans. The patterns of 81 genetic structure and diversity of populations are influenced by both historical and human- 82 mediated contemporary factors that determine changes in population size and gene flow 83 (Vucetich & Waite, 2003; Muhfeld et al., 2017), and that, ultimately, have driven the current 84 genetic patterns found in Moroccan trout. Therefore, to understand how the genetic structure, 85 diversity and demography of Moroccan trout populations have been shaped along its 86 evolutionary history, it is essential to consider on the one side the complex geomorphological 87 landscape of the High Atlas Mountains with its rivers flowing between steep canyons and the 88 climatic events that cause drastic floods in Morocco, that is a result of high tectonic activity 89 occurred during the Neogene and Quaternary eras (Michard, Frizon de Lamotte, Saddiqi & 90 Chalouan, 2008; Babault, Van den Driessche & Texeill, 2012; El Fels, Alaa, Bachnou & 91 Rachidi, 2018), and on the other side contemporary factors related to human activity in this 92 country. This complex geological history of Morocco has generated its highly diverse 93 mountains and river basins, and their highly isolated streams. Therefore, a high level of 94 genetic structure is expected in Moroccan trout since the formation of these freshwater 95 ecosystems. 96 Contemporary factors related to human activity are increasingly crucial to understand 97 current genetic structure and diversity of Moroccan trout populations. Aquatic resources are 98 being damaged worldwide due to increased infrastructure construction and overexploitation of 99 these resources for
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