Comparative sialomics between hard and soft ticks: Implications for the evolution of blood-feeding behavior

Abstract

Ticks evolved various mechanisms to modulate their host's hemostatic and immune defenses. Differences in the anti-hemostatic repertoires suggest that hard and soft ticks evolved anti-hemostatic mechanisms independently, but raise questions on the conservation of salivary gland proteins in the ancestral tick lineage. To address this issue, the sialome (salivary gland secretory proteome) from the soft tick, Argas monolakensis, was determined by proteomic analysis and cDNA library construction of salivary glands from fed and unfed adult female ticks. The sialome is composed of approximately 130 secretory proteins of which the most abundant protein folds are the lipocalin, BTSP, BPTI and metalloprotease families which also comprise the most abundant proteins found in the salivary glands. Comparative analysis indicates that the major protein families are conserved in hard and soft ticks. Phylogenetic analysis shows, however, that most gene duplications are lineage specific, indicating that the protein families analyzed possibly evolved most of their functions after divergence of the two major tick families. In conclusion, the ancestral tick may have possessed a simple (few members for each family), but diverse (many different protein families) salivary gland protein domain repertoire.

Evolution of the tissue factor pathway inhibitor-like Kunitz domain-containing protein family in Rhipicephalus microplus

“…Lineage-specific expansion of the Kunitz protein family has been previously observed in all studied ticks (Valenzuela et al, 2002;Francischetti et al, 2005Francischetti et al, , 2008aRibeiro et al, 2006;Alarcon-Chaidez et al, 2007;Batista et al, 2008;Chmelař et al, 2008;Mans et al, 2008a;Dai et al, 2012). Previous studies have shown that this protein family has evolved through gene duplication within the main tick families but after the divergence of hard and soft ticks (Mans et al, 2002b(Mans et al, , 2008aMans and Neitz, 2004).…”

“…Such expansions are present in both hard and soft ticks but are lineagespecific as they occurred after the divergence of the major tick families. They therefore coincided with the independent adaptation of the hard and soft ticks to a blood-feeding environment (Mans et al, 2002b(Mans et al, , 2008aMans and Neitz, 2004). Such adaptations would have required the evolution of proteins with novel functions that could facilitate blood-feeding behaviour and this was likely the evolutionary stimulus that resulted in the expansion of so many secretory protein families.…”

“…These lineage-specific expansions likely occurred during individual adaptations of hard and soft ticks to blood-feeding behaviour after their divergence from the ancestral tick (Mans et al, 2002b(Mans et al, , 2008aMans and Neitz, 2004). It is apparent that the Kunitz protein families are of integral importance to the haematophagous lifestyle of both hard and soft ticks.…”

“…Hard ticks possess more family members than the soft ticks (Mans et al, 2008a). The additional family members in hard ticks could have evolved in response to the long-term blood-feeding behaviour of the Ixodidae (Dai et al, 2012).…”

“…Previous studies have shown that this protein family has evolved through gene duplication within the main tick families but after the divergence of hard and soft ticks (Mans et al, 2002b(Mans et al, , 2008aMans and Neitz, 2004). The Kunitz protein family has therefore expanded in response to the blood-feeding environment that the Ixodidae and Argasidae encountered individually.…”