Their young bite better: On- and off-host selection pressure as drivers for evolutionary-developmental modification in Rhipicephalus ticks Deon K. Bakkes a, b, * , Dikeledi E. Matloa a , Ben J. Mans a, c, d , Conrad A. Matthee b a Gertrud Theiler Tick Museum, Epidemiology, Parasites and Vectors, Agricultural Research Council, Onderstepoort Veterinary Research, Pretoria, 0110, South Africa b Evolutionary Genomics Group, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa c Department of Veterinary Tropical Diseases, University of Pretoria, Pretoria, South Africa d Department of Life and Consumer Sciences, University of South Africa, South Africa article info Article history: Received 23 February 2022 Accepted 27 May 2022 Available online xxx Keywords: Development Neoteny Host Tick Geometric morphometric abstract 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 accel- erated (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 e heterotopic neoteny), or is allo- metrically repatterned possibly by using highly abundant and active hosts (three-host species using small hosts at early life stages e 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. © 2022 Elsevier Ltd. All rights reserved. 1. Introduction Development of organisms (ontogeny) results from genotypes that become expressed in phenotypes over the lifespans of organ- isms. Development has genetic and epigenetic bases that are her- itable and organised by developmental gene regulatory networks (Young and Badyaev, 2007; Klingenberg, 2010). Variation in development is an important source of evolutionary novelty (Love, 2006; Moczek, 2008; Ostachuk, 2016), driven by internal and external factors (Zelditch and Fink, 1996; Zelditch et al., 2003), that provide building blocks for phenotypic changes by selection or drift (Goldberg et al., 1991; True and Haag, 2001; Frankino et al., 2005). Morphological disparities (Drake and Klingenberg, 2010) between species can increase or decrease through development due to evolutionary changes in developmental phenotypes (McKinney and McNamara, 1991; McNamara and McKinney, 2005; Sheets and Zelditch, 2013) and some evidence demonstrates shape dis- parities tend to decrease through development, making adult * Corresponding author. Gertrud Theiler Tick Museum, Epidemiology, Parasites and Vectors, Agricultural Research Council, Onderstepoort Veterinary Research, Pretoria, 0110, South Africa. E-mail addresses: BakkesD@arc.agric.za, seventiaguitarist@gmail.com (D.K. Bakkes). Contents lists available at ScienceDirect Arthropod Structure & Development journal homepage: www.elsevier.com/locate/asd https://doi.org/10.1016/j.asd.2022.101189 1467-8039/© 2022 Elsevier Ltd. All rights reserved. Arthropod Structure & Development 70 (2022) 101189