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

Fabien L Condamine; Jonathan Rolland; Sebastian Höhna; Felix A H Sperling; Isabel Sanmartín

doi:10.1093/sysbio/syy009

Running with the Red Queen: the role of biotic conflicts in evolution

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2014.1382 ◽

2014 ◽

Vol 281 (1797) ◽

pp. 20141382 ◽

Cited By ~ 129

Author(s):

Michael A. Brockhurst ◽

Tracey Chapman ◽

Kayla C. King ◽

Judith E. Mank ◽

Steve Paterson ◽

...

Keyword(s):

Interspecific Interactions ◽

Red Queen Hypothesis ◽

Red Queen ◽

Evolutionary Forces ◽

The Face ◽

New Interactions ◽

Over 40 Years ◽

The Red Queen ◽

Early Phases

What are the causes of natural selection? Over 40 years ago, Van Valen proposed the Red Queen hypothesis, which emphasized the primacy of biotic conflict over abiotic forces in driving selection. Species must continually evolve to survive in the face of their evolving enemies, yet on average their fitness remains unchanged. We define three modes of Red Queen coevolution to unify both fluctuating and directional selection within the Red Queen framework. Empirical evidence from natural interspecific antagonisms provides support for each of these modes of coevolution and suggests that they often operate simultaneously. We argue that understanding the evolutionary forces associated with interspecific interactions requires incorporation of a community framework, in which new interactions occur frequently. During their early phases, these newly established interactions are likely to drive fast evolution of both parties. We further argue that a more complete synthesis of Red Queen forces requires incorporation of the evolutionary conflicts within species that arise from sexual reproduction. Reciprocally, taking the Red Queen's perspective advances our understanding of the evolution of these intraspecific conflicts.

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Testing the role of the Red Queen and Court Jester as drivers of the macroevolution of Apollo butterflies

10.1101/198960 ◽

2017 ◽

Author(s):

Fabien L. Condamine ◽

Jonathan Rolland ◽

Sebastian Höhna ◽

Felix A. H. Sperling ◽

Isabel Sanmartín

Keyword(s):

Large Scale ◽

Abiotic Factors ◽

Rapid Development ◽

Environmental Drivers ◽

Morphological Evidence ◽

Red Queen ◽

Extrinsic Factors ◽

Positive Dependence ◽

The Red Queen

AbstractIn 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 two types of factors to the evolutionary history of a lineage. Here 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 a 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.

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Getting somewhere with the Red Queen: chasing a biologically modern definition of the hypothesis

Biology Letters ◽

10.1098/rsbl.2017.0734 ◽

2018 ◽

Vol 14 (5) ◽

pp. 20170734 ◽

Cited By ~ 14

Author(s):

Luke C. Strotz ◽

Marianna Simões ◽

Matthew G. Girard ◽

Laura Breitkreuz ◽

Julien Kimmig ◽

...

Keyword(s):

Conceptual Understanding ◽

Biotic Interactions ◽

Population Level ◽

Red Queen Hypothesis ◽

Red Queen ◽

Evolutionary Patterns ◽

Evolutionary Theories ◽

Definition Of ◽

The Red Queen

The Red Queen hypothesis (RQH) is both familiar and murky, with a scope and range that has broadened beyond its original focus. Although originally developed in the palaeontological arena, it now encompasses many evolutionary theories that champion biotic interactions as significant mechanisms for evolutionary change. As such it de-emphasizes the important role of abiotic drivers in evolution, even though such a role is frequently posited to be pivotal. Concomitant with this shift in focus, several studies challenged the validity of the RQH and downplayed its propriety. Herein, we examine in detail the assumptions that underpin the RQH in the hopes of furthering conceptual understanding and promoting appropriate application of the hypothesis. We identify issues and inconsistencies with the assumptions of the RQH, and propose a redefinition where the Red Queen's reign is restricted to certain types of biotic interactions and evolutionary patterns occurring at the population level.

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