Structural and biochemical studies of the severe acute respiratory syndrome (SARS)-CoV-2 spike glycoproteins and complexes with highly potent antibodies have revealed multiple conformation-dependent epitopes highlighting conformational plasticity of spike proteins and capacity for eliciting specific binding and broad neutralization responses. In this study, we used coevolutionary analysis, molecular simulations, and perturbation-based hierarchical network modeling of the SARS-CoV-2 spike protein complexes with a panel of antibodies targeting distinct epitopes to explore molecular mechanisms underlying binding-induced modulation of dynamics and allosteric signaling in the spike proteins. Through coevolutionary analysis of the SARS-CoV-2 spike proteins, we identified highly coevolving hotspots and functional clusters that enable a functional cross-talk between distant allosteric regions in the SARS-CoV-2 spike complexes with antibodies. Coarse-grained and all-atom molecular dynamics simulations combined with mutational sensitivity mapping and perturbation-based profiling of the SARS-CoV-2 receptor-binding domain (RBD) complexes with CR3022 and CB6 antibodies enabled a detailed validation of the proposed approach and an extensive quantitative comparison with the experimental structural and deep mutagenesis scanning data. By combining in silico mutational scanning, perturbation-based modeling, and network analysis of the SARS-CoV-2 spike trimer complexes with H014, S309, S2M11, and S2E12 antibodies, we demonstrated that antibodies can incur specific and functionally relevant changes by modulating allosteric propensities and collective dynamics of the SARS-CoV-2 spike proteins. The results provide a novel insight into regulatory mechanisms of SARS-CoV-2 S proteins showing that antibody-escaping mutations can preferentially target structurally adaptable energy hotspots and allosteric effector centers that control functional movements and allosteric communication in the complexes.