Testing the Role of the Red Queen and Court Jester as Drivers of the Macroevolution of Apollo Butterflies

Abstract

In macroevolution, the Red Queen (RQ) model posits that biodiversity dynamics depend mainly on species-intrinsic biotic factors such as interactions among species or life-history traits, while the Court Jester (CJ) model states that extrinsic environmental abiotic factors have a stronger role. Until recently, a lack of relevant methodological approaches has prevented the unraveling of contributions from these 2 types of factors to the evolutionary history of a lineage. Herein, we take advantage of the rapid development of new macroevolution models that tie diversification rates to changes in paleoenvironmental (extrinsic) and/or biotic (intrinsic) factors. We inferred a robust and fully-sampled species-level phylogeny, as well as divergence times and ancestral geographic ranges, and related these to the radiation of Apollo butterflies (Parnassiinae) using both extant (molecular) and extinct (fossil/morphological) evidence. We tested whether their diversification dynamics are better explained by an RQ or CJ hypothesis, by assessing whether speciation and extinction were mediated by diversity-dependence (niche filling) and clade-dependent host-plant association (RQ) or by large-scale continuous changes in extrinsic factors such as climate or geology (CJ). For the RQ hypothesis, we found significant differences in speciation rates associated with different host-plants but detected no sign of diversity-dependence. For CJ, the role of Himalayan-Tibetan building was substantial for biogeography but not a driver of high speciation, while positive dependence between warm climate and speciation/extinction was supported by continuously varying maximum-likelihood models. We find that rather than a single factor, the joint effect of multiple factors (biogeography, species traits, environmental drivers, and mass extinction) is responsible for current diversity patterns and that the same factor might act differently across clades, emphasizing the notion of opportunity. This study confirms the importance of the confluence of several factors rather than single explanations in modeling diversification within lineages.

The contribution of temperature and continental fragmentation to amphibian diversification

“…Identifying the relative effect of different environmental factors to clades' diversification is an emerging goal in macroevolution (Benton, 2015;Condamine et al, 2012Condamine et al, , 2018Ezard et al, 2011;Roalson & Roberts, 2016). In this context, it is important to combine palaeontological and phylogenetic approaches and to test a wide range of diversification models.…”

“…Factors affecting the diversification of lineages are often placed in two categories: (a) the abiotic factors (Barnosky, 2001) and (b) the biotic factors (Van Valen, 1973). Thanks to recent methodological developments, the relative contribution of abiotic and biotic factors to the variation of speciation and extinction rates has been assessed in various groups using fossil data (Ezard, Aze, Pearson, & Purvis, 2011;Lehtonen et al, 2017;Liow, Reitan, & Harnik, 2015;Roalson & Roberts, 2016;Silvestro, Antonelli, Salamin, & Quental, 2015) or phylogenetic data (Condamine, Rolland, Höhna, Sperling, & Sanmartín, 2018;Condamine, Sperling, Wahlberg, Rasplus, & Kergoat, 2012;Lagomarsino, Condamine, Antonelli, Mulch, & Davis, 2016;Pérez-Escobar et al, 2017).…”

“…On the contrary, Jordan et al (2016) concluded that continental drift is not sufficient to account for the increase in terrestrial species richness observed in the fossil record. Tectonic changes have also been examined recently by studies evaluating the effect of mountain orogeny on diversification using phylogenies of plants (Lagomarsino et al, 2016;Pérez-Escobar et al, 2017) and animals (Condamine et al, 2018;Xu, Kuntner, Liu, Chen, & Li, 2018).…”

“…Although the role of temperature has been already tested in several clades (Condamine, Rolland, & Morlon, 2013;Condamine et al, 2018;Pyron & Wiens, 2013;Roalson & Roberts, 2016), the link between diversification and continental fragmentation remains seldom tested empirically with birth-death models. Recent developments in the field of diversification models permit to assess the role of variables that vary through time on the diversification processes (Condamine et al, 2013;Morlon et al, 2016).…”

Ancient tropical extinctions contributed to the latitudinal diversity gradient

“…The new temperate habitats could have constituted an opportunity for diversification because they increased geographic ranges and ecological niches 31 , and may have eventually driven an inverse LDG for some groups 37,84 . Several radiations following the appearance of the temperate biome have been identified in other groups of organisms, such as plants 83,85 , mammals 86,87 or insects 88 . After this period, speciation decreased dramatically in the temperate lineages of our focal groups, possibly due to the effect of the Pleistocene glaciations, and we estimated similar diversification rates between tropical and temperate lineages (Fig.…”