Their young bite better: On- and off-host selection pressure as drivers for evolutionary-developmental modification in Rhipicephalus ticks.

Distinct life stages may experience different selection pressures influencing phenotypic evolution. Morphological evolution is also constrained by early phenotypes, since early development forms the phenotypic basis of later development. This work investigates evolutionary-developmental modification in three life stages and both sexes of 24 Rhipicephalus species using phylogenetic comparative methods for geometric morphometrics of basis capituli (basal mouthpart structure used for host attachment), and scutum or conscutum areas (proxy for overall body size). Findings indicate species using large hosts at early life stages have distinct basis capituli shapes, correlated with host size, enabling attachment to the tough skins of large hosts. Host-truncate species (one- and two-host) generally retain these adaptive features into later life stages, suggesting neoteny is linked to the evolution of host truncation. In contrast, species using small hosts at early life stages have lost these features. Developmental trajectories differ significantly between host-use strategies (niches), and correlate with distinct clades. In two-host and three-host species using large hosts at early life stages, developmental change is heterotopically accelerated (greater cell mass development) before the first off-host period where selection probably favours large individuals able to better resist dehydration when questing (waiting) for less abundant, less active hosts. In other species, development is heterotopically reduced (neotenic), possibly because dehydration risk is bypassed by prolonged host attachment (one-host species - heterotopic neoteny), or is allometrically repatterned possibly by using highly abundant and active hosts (three-host species using small hosts at early life stages - allometric repatterning). These findings highlight complex trade-offs between on- and off-host factors of free-living ectoparasite ecology, which mediate responses to diverse selection pressures varied by life stage and host-use strategy. It is proposed that these trade-offs shape evolutionary-developmental morphology and diversity of Rhipicephalus ticks.

Adaptive radiation and speciation in Rhipicephalus ticks: A medley of novel hosts, nested predator-prey food webs, off-host periods and dispersal along temperature variation gradients.

Rhipicephalus are a species-diverse genus of ticks, mainly distributed in the Afrotropics with some species in the Palearctic and Oriental regions. Current taxonomic consensus comprise nine informal species groups/lineages based on immature morphology. This work integrates biogeographic, ecological and molecular lines of evidence to better understand Rhipicephalus evolution. Phylogenetic analysis based on four genes (12S, 16S, 28S-D2 and COI) recovered five distinct clades with nine descendant clades that are generally congruent with current taxonomy, with some exceptions. Historical biogeography is inferred from molecular divergence times, ancestral distribution areas, host-use and climate niches of four phylogenetically significant bioclimatic variables (isothermality, annual, seasonal and diurnal temperature range). Novel hosts enabled host-linked dispersal events into new environments, and ticks exploited new hosts through nested predator-prey connections in food webs. Diversification was further induced by climate niche partitioning along gradients in temperature range during off-host periods. Ancestral climate niche estimates corroborated dispersal events by indicating hypothetical ancestors moved into environments with different annual and seasonal temperature ranges along latitudinal gradients. Host size for immature and adult life stages was important for dispersal and subsequent diversification rates. Clades that utilise large, mobile hosts (ungulates and carnivores) early in development have wider geographic ranges but slower diversification rates, and those utilising small, less mobile hosts (rodents, lagomorphs and afroinsectivores) early in development have smaller ranges but higher diversification rates. These findings suggest diversification is driven by a complex set of factors linked to both host-associations (host size, ranges and mobility) and climate niche partitioning along annual and seasonal temperature range gradients that vary with latitude. Moreover, competitive interactions can reinforce these processes and drive speciation. Off-host periods facilitate adaptive radiation by enabling host switches along nested predator-prey connections in food webs, but at the cost of environmental exposure that partitions niches among dispersing progenitors, disrupting geneflow and driving diversification. As such, the evolution and ecological niches of Rhipicephalus are characterised by trade-offs between on- and off-host periods, and these trade-offs interact with nested predator-prey connections in food webs, host-use at different life stages, as well as gradients in annual and seasonal temperature ranges to drive adaptive radiation and speciation.