Adaptive Evolution Of Waterfleas To Cyanobacterial Blooms In Urbanized Waters

Populations can respond to changing environments through migration,phenotypic plasticity,and evolution.Understanding whether populations can adapt to environmental changes is a core issue in evolutionary biology.Urban construction causes severe habitat loss and fragmentation.These effects are particularly pronounced in aquatic systems.For example,urban construction will reduce the connectivity of river networks,form many small water bodies,and increase habitat heterogeneity.The main purpose of this study is to investigate whether environmental changes caused by urbanization promote microgeographic adaptation.It mainly includes the following contents:The eutrophication and cyanobacteria blooms caused by urbanization are threatening the ecological environments and ecosystem services on a global scale.Exploring how organisms adapt to rapid environmental changes is important for understanding the evolutionary fate of populations and the future of biodiversity.In aquatic ecosystems,the interactions between zooplankton and phytoplankton play a critical role in transferring carbon from primary producers to higher trophic levels and provide an ecological function of top-down control of phytoplankton blooms.In this study,we investigated whether urbanization resulted in microgeographic adaptation and quantified the relative contribution of phenotypic plasticity and genetic changes(including constitutive evolution and evolution of plasticity)to overall trait changes using Ceriodaphnia cornuta as a model species.Based on the developed microsatellite loci,genetic analysis was performed on nine C.cornuta populations with a spatial span of 60 km in the Huangpu River to explore the fine-scale genetic structure in the river landscapes.Using the common garden experiment,we quantified the multivariable reaction norms of different geographic populations to cyanobacteria.The results showed that the degree of urbanization was positively correlated with the microcystin concentration in the surface sediment of each sampling location in the Huangpu River,and the genetic differentiation between C.cornuta populations with different degrees of urbanization was significant at a microgeographic scale.Phenotypic plasticity and the evolution of plasticity play important roles in the overall trait changes.This study tested whether increasing levels of cyanobacteria led to multivariate reaction norm changes in a natural zooplankton population.After resurrecting dormant eggs of three C.cornuta sub-populations in the Dianshan Lake,a common garden experiment was carried out to quantify the multivariate reaction norms of nine morphological,life history and behavioral traits of C.cornuta when dealing with the toxic cyanobacterium Microcystis aeruginosa.The most recent sub-population from the high eutrophication period was characterized by smaller size at birth and maturity,and releasing fewer offspring in their second brood compared with the ancient subpopulation from the low eutrophication period.Covariant patterns in multivariate trait space provided strong evidence of adaptive evolution in multiple traits over time.The total trait change generated through both evolution and the evolution of plasticity ranged from 1% to 64% depending on the trait and sub-population comparison while phenotypic plasticity contributed the most(22% to 86%).These results suggest that the study population rapidly tracked environmental changes through integrating plasticity,evolution of trait means and evolution of plasticity to achieve multivariate phenotypic shifts.Previous studies on rapid adaptation have mainly focused on how specific natural selection pressures drive the evolution of populations,but little is known about the evolutionary consequences of the weakening or disappearance of natural selection pressures(ie,"relaxed selection").After the partial isolation from the Yingtao River by urban construction 16 years ago,the cyanobacterial abundance in the Shangyi Pond has decreased significantly due to no longer being polluted by urban wastewater.Genetic analyses using nuclear microsatellite loci revealed significant population genetic structure among C.cornuta populations.Migration analyses demonstrated little gene flow among different waters.The changes in multivariate reaction norms provided evidence that local adaptation to dietary cyanobacteria in the Shangyi Pond has been reversed.Whether the presence of toxic cyanobacteria and subsequent removal can lead to rapid forward and reverse genetic changes in multiple traits of C.cornuta was tested using experimental evolution.In the selection experiment,the covariant pattern in multivariate trait space provided strong evidence of adaptive evolution in multiple traits at two selection levels with the presence of toxic cyanobacteria.The C.cornuta populations from the high selection level showed the higher tolerance than these from the low selection level.The total trait change generated through evolutionary responses(constitutive evolution and evolution of plasticity)ranged from 0% to 32% depending on the trait and selection level.In the relaxation experiment,almost all evolved traits were restored to their original state when C.cornuta were fed pure green algae.The genotypes dynamics indicated that asymmetric intraspecific competition may be the main force driving the rapid reverse evolution.The results suggest that environmental switch between proliferation and decrease of cyanobacteria resulted in rapid forward and reverse evolution of multivariate phenotypic responses in grazer C.cornuta.These results have important implications for applied biology,such as reversing some evolutionary responses that are adverse to ecosystem services(e.g.,evolution of pathogen resistance and smaller size at maturation in fish).