First evidence of a genetic basis for thermal adaptation in a schistosome host snail

Abstract

Freshwater snails play a key role in the transmission of schistosomiasis, a tropical parasitic disease affecting over 150 million people. Adaptation of these snails to local climatic conditions is a critical factor in determining how climate change and other environmental factors influence disease transmission dynamics, yet this potential adaptation has remained unexplored. Bulinus truncatus is the schistosome intermediate host snail with the widest geographic distribution and is therefore an important factor 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 (N = 2304) was exposed to eight chronic temperature treatments (±36 snails/population/temperature treatment) and various life history traits were recorded for over 14 weeks. Subsequently, ecophysiological analyses were conducted on the 10 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 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 hemoglobin contents in cold-adapted snails. In contrast, warm-adapted snails displayed not only increased protein levels but also more oxidative damage. Furthermore, heightened phenoloxidase levels indicated a more robust immune response in snails from parasite-rich regions. These morphological and physiological differences provide convincing evidence for a genetic basis of local adaptation. This in turn holds profound implications for the snail's response to climate change, future schistosomiasis risk, and the effectiveness of schistosomiasis control measures.