1. Introduction
Vector-borne parasites are common, important biological enemies of humans, animals, and plants, transmitted by one living organism to another. Despite the recent gains in reducing the overall global burden for parasites like malaria (Gething et al. 2010; Bhatt et al. 2015; Ashepet et al. 2021), vector-borne diseases still account for 17% of all infectious diseases and cause 700,000 deaths in humans annually (W.H.O. 2020). Livestock and crop systems are also plagued by vector-borne diseases, which place serious constraints on agricultural production globally (Döring 2017; Garros et al.2017), and vector-borne diseases can be devastating in wildlife populations, particularly when introduced to new areas. Collectively, tens of billions of dollars are spent every year on control, medical interventions, and mitigating loss of productivity (Warner 1968; Georgeet al. 2015; Stuchin et al. 2016; Aguirre 2017; Weaveret al. 2018).
The dependence of many pathogens on ectothermic arthropod vectors for transmission means that vector-borne diseases are highly sensitive to variation in the environment. Arthropod vectors experience a complex suite of environmental factors, both abiotic (e.g., temperature, rainfall, humidity, salinity) and biotic (e.g., biological enemies, inter- and intra-specific interactions, and variation in habitat quality). These factors vary in their relative effects on organismal fitness, can synergize (Kleynhans & Terblanche 2011; Huxley et al. 2021, 2022; Liu & Gaines 2022), and exert their effects at different spatial scales (Cohen et al. 2016) with important consequences for the abundance and distribution of arthropod vectors (Ryan et al. 2015; Evans et al. 2019), vector population dynamics (Murdock et al. 2017), and pathogen transmission (Samuelet al. 2011; Mordecai et al. 2013; Murdock et al.2014a, 2016; Mordecai et al. 2017; Huber et al. 2018; Shocket et al. 2018b; Tesla et al. 2018; Wimberly et al. 2020; Ngonghala et al. 2021).
In vector ecology, there has been a strong emphasis on studying the effects of temperature on mosquito-borne pathogen transmission (reviewed in Mordecai et al. 2019). In addition to temperature, water availability is another critical abiotic variable influencing ectotherm biology, and both play important roles determining the distribution and abundance of ectotherms (Chown & Nicolson 2004; Deutsch et al.2008; Steiner et al. 2008; Kearney & Porter 2009; Roura-Pascualet al. 2011; Lenhart et al. 2015; Rozen-Rechels et al. 2019; González-Tokman et al. 2020; Klink et al. 2020) and species richness (Jamieson et al. 2012; Calatayud et al. 2016; Beck et al. 2017; Cardoso et al. 2020; Pilottoet al. 2020; Hamann et al. 2021). Body temperature has important effects on the rates of enzymatic processes as well as the structural integrity of cellular membranes and proteins (Angilletta 2009), while all cellular processes rely on water as a solvent for biochemical reactions and for trafficking nutrients into, within, and out of cells (Chown & Nicolson 2004; Chaplin 2006). Temperature also affects the amount of desiccation stress an organism experiences due to the fundamental relationship between ambient temperature and the amount of water the surrounding air can hold (Lawrence 2005; Romps 2021). Other fields at the climate-health interface have explored the effects of wet heat vs dry heat on the energy budgets of endotherms in the context of human heat stress and climate change (Buzan & Huber 2020). We anticipate that variation in relative humidity is also an important force shaping the thermal performance of ectotherms, including mosquitoes. Whereas metabolic theory has been well developed and widely applied in ecology to understand temperature effects (Brown et al. 2004; Dell et al. 2011; Corkrey et al. 2016) we currently lack a similar framework for understanding how humidity and temperature interact to influence mosquitoes and their pathogens.
In this Perspectives, we explore the effects of humidity on the thermal performance of mosquito-borne pathogen transmission. We begin by summarizing what is currently known about how temperature and humidity affects mosquito fitness, population dynamics, and pathogen transmission, whilst highlighting current knowledge gaps. We present a conceptual framework for understanding the interaction between temperature and humidity and how it shapes the range of temperatures across which mosquitoes persist and achieve high transmission potential. We then discuss how failing to account for these interactions across climate variables hinders efforts to forecast transmission dynamics and to respond to epidemics of mosquito-borne infections. We end by outlining future research areas that will ground the effects of humidity on thermal performance of pathogen transmission in a theoretical and empirical basis to improve spatial and temporal prediction of vector-borne pathogen transmission. Such a framework will inform multiple fields (thermal, disease, and landscape ecology and epidemiology) and a diversity of vector-borne disease systems (human, wildlife, domestic animals, and plants).