Large-Scale Modelling of the Environmentally-Driven Population Dynamics of Temperate Aedes albopictus (Skuse)

Abstract

The Asian tiger mosquito, Aedes albopictus, is a highly invasive vector species. It is a proven vector of dengue and chikungunya viruses, with the potential to host a further 24 arboviruses. It has recently expanded its geographical range, threatening many countries in the Middle East, Mediterranean, Europe and North America. Here, we investigate the theoretical limitations of its range expansion by developing an environmentally-driven mathematical model of its population dynamics. We focus on the temperate strain of Ae. albopictus and compile a comprehensive literature-based database of physiological parameters. As a novel approach, we link its population dynamics to globally-available environmental datasets by performing inference on all parameters. We adopt a Bayesian approach using experimental data as prior knowledge and the surveillance dataset of Emilia-Romagna, Italy, as evidence. The model accounts for temperature, precipitation, human population density and photoperiod as the main environmental drivers, and, in addition, incorporates the mechanism of diapause and a simple breeding site model. The model demonstrates high predictive skill over the reference region and beyond, confirming most of the current reports of vector presence in Europe. One of the main hypotheses derived from the model is the survival of Ae. albopictus populations through harsh winter conditions. The model, constrained by the environmental datasets, requires that either diapausing eggs or adult vectors have increased cold resistance. The model also suggests that temperature and photoperiod control diapause initiation and termination differentially. We demonstrate that it is possible to account for unobserved properties and constraints, such as differences between laboratory and field conditions, to derive reliable inferences on the environmental dependence of Ae. albopictus populations.

Fig 1. The stage- and age-structured time-difference equations model of Ae. albopictus.

Fig 2. Relative support for the inferred higher-probability posterior modes.

Expected posterior probabilities of the selected modes, $\mathcal{S}=\{\Theta 1\dots \Theta 3\}$, are shown against a range of tolerance values, T_tol.

Fig 3. Performance evaluation against the surveillance data from Emilia-Romagna.

Blue diamonds represent average egg counts per ovitrap, and vertical error bars represent the standard error of the mean. They are positioned at the dates of data collection along the horizontal axis. Blue bars in the background indicate the number of ovitraps covering a period of two weeks prior to each collection. Solid black lines show model output using the parameters from Θ1 (see text). Red shades represent the 95% confidence interval.

Fig 4. Sensitivity analysis for Θ1.

The bar chart displays the logarithm of sensitivity, ${\mathcal{H}}_{\theta }$, along the set of parameter dimensions included in the inference.

Fig 5. Cold resistance for adults and diapausing eggs with Θ1.

Prior (blue) and posterior (red) distributions of diapausing eggs (a) and adult females (b) are shown with data from literature (numbered circles). The prior distribution is represented by a solid line (mean) and a shaded region (95% confidence interval). The posterior distribution is represented by 100 samples drawn from the posterior mode Θ1. Daily average diapausing eggs (c) and adult females (d) per ovitrap are simulated with Θ1. The solid line represents the mean and the red shade represents the 95% confidence interval. (a) 1: [52], (b) 1: [71], 2: [72], 3: [58], 4: [46], 5: [73], 6: [74], 7: [75], 8: [76], 9: [77], 10: [78], 11: [79], 12: [80].

Fig 6. Habitat suitability indices (HSI) for Europe with Θ1.

The indices are shown for the available grid points of the environmental datasets as described in the text. Each value indicates the expected fold change compared to the reference index (RSI) obtained over Emilia-Romagna.