First evidence of a causal link between genetic variation and thermal adaptation in a schistosome host snail

Abstract

Freshwater snails are pivotal in transmitting schistosomiasis, a tropical parasitic disease affecting over 150 million people. The adaptive potential of these snails is a critical factor in determining how climate change and other environmental factors influence disease transmission dynamics, yet it has remained unexplored. Bulinus truncatus is the schistosome intermediate host snail with the widest geographic distribution and therefore plays a pivotal role in determining the maximum range of urogenital schistosomiasis. In this study, we assessed the local adaptation capacity of B. truncatus to temperature through an integrative approach encompassing phenotypic, ecophysiological, and genomic data. Ten snail populations from diverse thermal environments were collected in three countries, with eight populations reared in a common garden. The F2 generation (total N= 2592) was exposed to eight chronic temperature treatments and various life-history traits were recorded for over 14 weeks. Subsequently, ecophysiological analyses were conducted on the ten last surviving snails per population. Genotyping the parental generation collected in the field using a genotyping-by-sequencing (GBS) approach, revealed 12,875 single nucleotide polymorphisms (SNPs), of which 4.91 % were potentially under selection. We observed a significant association between these outlier SNPs, temperature, and precipitation. Thermal adaptations in life-history traits were evident, with lower survival rates at high temperatures of warm- origin snails compensated for by higher reproduction rates. Cold-origin snails, on the other hand, exhibited higher growth rates adapted to a shorter growing season. Ecophysiological adaptations included elevated sugar and haemoglobin contents in cold-adapted snails. In contrast, warm-adapted snails displayed increased protein levels but also more oxidative damage. Furthermore, heightened phenoloxidase levels indicated a more robust immune response in snails from parasite-rich regions. The substantial local adaptation capacity of B. truncatus holds profound implications for its response to climate change, future schistosomiasis risk, and the effectiveness of schistosomiasis control measures. HighlightsO_LILocal adaptation influences species responses to climate change C_LIO_LIThe snail Bulinus truncatus showed a high thermal local adaptation (LA) potential C_LIO_LILA is apparent through variations in life history and ecophysiological traits C_LIO_LIWe identified a significant genetic basis underlying this LA C_LIO_LILA of the hosts could sustain schistosomiasis transmission under global warming C_LI