| Genetic diversity is the bedrock of adaptation to environmental changes,and it is also an important reference to assess the evolutionary potential of populations.According to “Genetic erosion hypothesis”,environmental heavy metal pollution may be one of the important factors for the decreased genetic diversity in natural populations.Related studies have focused on invertebrates or lower vertebrates,but whether similar phenomena may also occur in higher vertebrate—birds have not been reported.Moreover,extra-pair copulation is widespread in socially monogamous bird populations,which not only has important adaptive significance for the sexes,but also is closely related to the population genetic diversity.However,few studies have reported the variation and intrinsic connection of genetic diversity and extra-pair copulation under environmental heavy metal pollution.The study selected socially monogamous tree sparrow(Passer montanus),a kind of resident bird,as study subject and Silong(SL)area of Baiyin in Gansu province as study site,which was mainly polluted by heavy metals Cu,Zn,Pb,Cd for more than60 years.Combined with the findings of our research group on the local environmental background values and home range of this species,Guanyinya(GYY),Minqin(MQ),Shuanghe(SH),Liangzhuang(LZ),Yongxing(YX)administrative villages with different levels of heavy metal pollution were selected as sampling points.Meanwhile,Weijiachuan(WJC)village of Liujiaxia(LJX)area in Linxia Hui Autonomous Prefecture,Gansu province was used as control sampling point.Seven highly polymorphic and stably amplified microsatellite loci were screened,and the relationship between environmental heavy metal pollution and genetic diversity of tree sparrow population was analyzed using these microsatellite markers and flame atomic absorption spectroscopy.In MQ sampling point of SL area with severe heavy metal pollution and relatively unpolluted WJC sampling point of LJX area,extra-pair copulation and inbreeding level were investigated;the fitness characteristics such as body parameters and standard heterozygosity in extra-pair offspring,within-pair offspring,extra-pair mates and social mates of female were analyzed to explore the response of female extra-pair copulation behavior to environmental heavy metal pollution;the adaptive role of male extra-pair copulation behavior was evaluated by analyzing their sperm traits.The main study results were as follows:1.Accumulation levels of environmental heavy metals in primary flight feathers of tree sparrows.Pb and Cd concentrations of tree sparrows from GYY,MQ,SH,LZ of SL area were significantly higher than those from WJC of LJX area(p <0.05),while GYY and MQ tree sparrow population living in the upstream of sewage ditch(Dongdagou)were more severely polluted with Cd and Pb than the other populations in SL area(p < 0.05).Tree sparrow populations from SL area showed different accumulations of heavy metals,and results can be conducive to investigating the response of genetic diversity and extra-pair copulation under similar natural factors but different heavy metal pollution levels.2.Effect of environmental heavy metal pollution on the genetic diversity of tree sparrow populations.GYY and MQ tree sparrow populations in SL area had lowest average allele richness(10.8756)and observed heterozygosity(0.7512)respectively,but they were not significantly different with those from the WJC tree sparrow population in LJX area(p > 0.05);observed heterozygosity and allelic richness were negatively correlated to the Pb and Cd concentrations in the primary flight feathers of tree sparrows(p < 0.05).These results indicated that the genetic diversity of tree sparrow populations was lower under environmental heavy metal pollution,and the enrichment of Pb and Cd may increase the risk of decreased genetic diversity.3.Effect of environmental heavy metal pollution on the genetic differentiation of tree sparrow populations.The Fst ranged between-0.00197 and0.01075,showing that the genetic differentiation level was low.The analysis of molecular variance showed that most of the genetic variation was from individuals,accounting for 99.24901% of the total variation,while genetic variation between groups(SL areas and WJC areas)and among populations within groups were low,accounting for 0.36444% and 0.38655% of the total variation,respectively.Above results indicated that environmental heavy metal pollution had no significant effect on genetic differentiation of tree sparrow populations.4.Variation in extra-pair copulation of tree sparrows under environmental heavy metal pollution.The number of extra-pair offspring in MQ tree sparrow population of SL area was significantly higher than that in WJC of LJX area(p =0.045),while there was no significant deviation in the sex ratio of extra-pair offspring from the two tree sparrow populations(MQ: p = 0.846;WJC: p = 0.581).These results showed that the incidence of extra-pair copulation was increased but the sexual ratio of extra-pair offspring was not biased to male in tree sparrow population exposed to environmental heavy metal pollution.5.Response of extra-pair copulation behavior of male tree sparrows to environmental heavy metal pollution.Compared with WJC of LJX area,the male tree sparrows from MQ population of SL area produced longer sperm(p = 0.004)with longer flagella(p = 0.002)and smaller head/flagellum ratios(p = 0.041),and the sperm velocity was higher.The sperm velocity and total sperm length of tree sparrows significantly affected their extra-pair fertilization success(p < 0.05).Male tree sparrows showed better sperm morphological characteristics and movement performance under environmental heavy metal pollution,and adaptive variation of sperm traits was closely related to the higher incidence of extra-pair copulation.6.Response of extra-pair copulation behavior of female tree sparrows to environmental heavy metal pollution.In MQ tree sparrow population of SL area,there was high degree of inbreeding between social mates,and body condition of female extra-pair mates was significantly better than their social mates(p = 0.046).Relatedness of extra-pair mates was lower than that of social mates,and the difference was close to significant(p = 0.052).Body condition,standard heterozygosity,body parameters,flight rate of extra-pair offspring were significantly higher than those of within-pair offspring(p < 0.05).However,these phenomena were not found in WJC tree sparrow population of LJX area.Above results showed that the extra-pair copulation behavior of females can not only improve offspring fitness,but also increase genetic diversity of population.In conclusion,environmental heavy metals can be accumulated in tree sparrows and had adverse effects on population genetic diversity.In addition,inbreeding was common in MQ tree sparrow population with severe heavy metal pollution,thereby increasing incidence of extra-pair copulation under this selection pressure.Because sperm velocity and total sperm length of male tree sparrows were essential for their extra-pair fertilization success,rapid evolution of these sperm traits happened in this population.Meanwhile,female tree sparrows also showed adaptive responses in extra-pair copulation strategies,and they tended to choose males with better body condition and lower relatedness as extra-pair mates to improve offspring fitness and population genetic diversity.Therefore,this study could provide a reference for probing the mechanisms of environmental pollution affecting genetic diversity in socially monogamous birds and the evolution of their extra-pair copulation strategies. |
PDF Full Text Request