Integrative research of sexual dimorphism evolution

Certain animal and plant lineages have independently evolved pronounced sexual dimorphism (SD) where the sexes significantly differ in size, shape, behavior, or physiology. Well-known vertebrates exhibit sexual size dimorphism (SSD) where males are the larger sex, but the more dramatic phenomenon is female-biased SSD in invertebrates where females may be up to 10,000 times the male’s weight. The evolution of SSD has been explained by sex-specific life histories optima, where males and females achieve higher fitness at different sizes. The female-biased SSD in arthropods likely evolved via fecundity selection, where female gigantism enables greater fitness through increased egg production and more viable offspring. On the other hand, the persistence of males at ancestral sizes is often explained by scramble competition for virgin females despite the expectation that male-male antagonism favors large body size. The complexity of selection pressures affecting male and female body sizes yielding sex-specific trade-offs between developmental time and adult size calls for more research, which may elucidate evolutionary causes as well as consequences of SD. 

Most studies have ignored phylogenies and simplified the explanations of processes and traits that lead to SSD, or result as its consequence. Identifying adaptive selection is particularly strong if a trait is shown to be independently acquired—or convergent. Convergence can help detect common evolutionary solutions. Our approach to studying SSD is through integration of phylogenetic, ecological, behavioral, developmental, evolutionary and phylogenomic methodology, an approach that will help us discern between evolutionary causes and consequences in two independent lineages. It has become clear that comparative phylogenetic works investigating macro-evolutionary patterns need to be married with experimental studies on model taxa investigating micro-evolutionary processes in order to elucidate the big pictures in evolution. Our proposal is the first to deliver this while studying the repeated evolution of traits that correlate with SSD.

Spiders evolved extreme SD several times and are ideal animals for comparative research, particularly considering seemingly bizarre sexually selected adaptations in highly dimorphic lineages; these include sexual cannibalism, male self-sacrifice, emasculation, genital plugging and infanticide. Higher level phylogenetics explains SSD in orb weavers primarily as female gigantism arising through fecundity selection, but looking at a finer taxonomic scale, the patterns are more complex and may be due to a combination of natural and sexual selection mechanisms. However, the lack of empirical data precludes definitive interpretations of the evolution and biological correlates of spider SD.

To obtain robust phylogenies for two spider groups representing evolutionary replicas of SD—golden orb weavers (Nephila, Nephilidae) and cross spiders (Argiope, Araneidae)—we propose to use next generation sequencing yielding nucleotide data that would augment our current sampling by two orders of magnitude. We will combine phylogenies with developmental, behavioral and evolutionary analyses in order to test six original hypotheses: 1 Size evolution is independent between the sexes; 2 Selection pressures, and size optima, differ between the sexes; 3 Evolution of female gigantism is constrained by development; 4 Evolutionary origins of SSD are confined to the tropics; 5 Female gigantism has common ecological and life history consequences; 6 Female gigantism has common behavioral and physiological consequences. The evidence from these hypotheses will ultimately help us to answer the question whether SD has predictable (co)evolutionary consequences. Our proposal has the potential to make significant progress in evolutionary biology, and advance Slovenia’s scientific excellence.