Transcriptomic imprints of adaptation to fresh water: parallel evolution of osmoregulatory gene expression in the Alewife

Abstract

Comparative approaches in physiological genomics offer an opportunity to understand the functional importance of genes involved in niche exploitation. We used populations of Alewife (Alosa pseudoharengus) to explore the transcriptional mechanisms that underlie adaptation to fresh water. Ancestrally anadromous Alewives have recently formed multiple, independently derived, landlocked populations, which exhibit reduced tolerance of saltwater and enhanced tolerance of fresh water. Using RNA-seq, we compared transcriptional responses of an anadromous Alewife population to two landlocked populations after acclimation to fresh (0 ppt) and saltwater (35 ppt). Our results suggest that the gill transcriptome has evolved in primarily discordant ways between independent landlocked populations and their anadromous ancestor. By contrast, evolved shifts in the transcription of a small suite of well-characterized osmoregulatory genes exhibited a strong degree of parallelism. In particular, transcription of genes that regulate gill ion exchange has diverged in accordance with functional predictions: freshwater ion-uptake genes (most notably, the 'freshwater paralog' of Na /K -ATPase α-subunit) were more highly expressed in landlocked forms, whereas genes that regulate saltwater ion secretion (e.g. the 'saltwater paralog' of NKAα) exhibited a blunted response to saltwater. Parallel divergence of ion transport gene expression is associated with shifts in salinity tolerance limits among landlocked forms, suggesting that changes to the gill's transcriptional response to salinity facilitate freshwater adaptation.

Understanding the molecular basis of adaptation to freshwater environments by prawns in the genus Macrobrachium

“…To date, osmoregulatory capacity is considered to be the principal mechanism for crustacean adaptation to freshwater (Faria et al, 2011;Brennan et al, 2015;Velotta et al, 2017). However, osmoregulation cannot be the sole mechanism for freshwater adaptation.…”

“…Tighter cell junctions are required for osmoregulation in freshwater compared with raised salinity conditions (Tipsmark et al, 2002;Brennan et al, 2015;Velotta et al, 2017). The intensity of selection pressure acts differently under different environmental conditions that in turn, can result in sequence divergence in the coding regions in a number of candidate genes controlling a specific phenotype while maintaining the sequences conserved in other genes (Ellegren, 2014;Berdan et al, 2015;Bailey and Bataillon, 2016 In a diverse array of crustacean species, regulation of internal body fluid content via haemolymph production is considered to be one of the principal mechanisms for maintaining an iso-osmotic body fluid concentration relative to the surrounding aquatic medium (McNamara et al, 2015;Mitterboeck et al, 2016).…”

“…Currently, change in osmoregulatory capacity is considered to be the principal mechanism for adaptation to different osmotic conditions (Lee and Bell, 1999;DeFaveri et al, 2011;Kozak et al, 2013;Velotta et al, 2017). Osmoregulation is not however, the only mechanism for freshwater adaptation; other mechanisms can also play important roles.…”

“…To date however, little work has been directed at identifying and characterizing genes and pathways that facilitated crustacean adaptation to freshwater environments. A number of studies of fish have concluded that changes to expression of osmoregulatory genes have played the principal roles in driving this process (DeFaveri et al, 2011;DeFaveri and Merila, 2014;Brennan et al, 2015;Velotta et al, 2015;Velotta et al, 2017). Crustaceans unlike most vertebrates often possess complex life cycles that involve many developmental stages in different habitats.…”

“…Currently, osmoregulation (primarily in the gill) is considered to be the principal mechanism by which aquatic species adapt to a wide ranging salinity gradients by maintaining the ionic balance between intra-and extra-cellular environments (McNamara et al, 2015;Rahi et al, 2017;Velotta et al, 2017). In a novel environment with different salinity level, efficient adaptation via osmoregulation depends on a combination of plastic morphological, physiological and genomic/genetic responses (Havird et al, 2014;Brennan et al, 2015;Velotta et al, 2015).…”