Sexual selection: patterns in the history of life

The evolution of sex, and its subsequent high prevalence in nature, is one of the great mysteries of life. The main reason, the so-called "twofold cost of sex", has something to do with male production: the cost does not exist in the same form in isogamous organisms that lack males and females. Such organisms, however, can still experience e.g. costs of mate-finding. The differences in costs are relevant because sex does not always coincide with there being two sexes in a population: ancient sex was neither obligatory nor did it feature a male-female dimorphism. This talk will discuss how this impacts the evolution of sex, and how the rules of sex change once there are males (a specialized morph that finds it more difficult to switch to asexual reproduction than what is possible for females).

The idea that sexual selection can promote speciation dates back to Darwin. However, relationships between speciation rates and proxies for sexual selection (e.g. mating system, sexual dimorphism) differ substantially between taxa, indicating that the contribution of sexual selection to speciation depends on the biology of the organism as well as its environment. One major explanatory variable concerns the interaction of sexual selection with other forms of selection. Specifically, direct effects of ecological adaptation on sexual communication are thought to be particularly powerful in generating and maintaining reproductive isolation – but how common are such direct effects? In this talk, Dr Maan will highlight the difference between direct vs indirect effects of ecological adaptation on sexual selection processes, and the importance of this distinction for speciation. Dr Maan will illustrate this point using her group’s ongoing work on sensory drive in cichlid fish, where visual adaptation to alternative light environments coincides with divergent mate preferences.

For the vast majority of Metazoans and many plants, evolution occurs via selection on genes expressed in two distinct subpopulations: males and females. Yet despite much interest in the evolution of sexual dimorphism, we know little about whether and why independent evolution of the sexes has affected the dynamics of diversification, impeding our understanding of the origins and maintenance of a substantial portion of biodiversity. In this paper we attempt reconcile the uncertain role that evolutionary divergence between the sexes may play in the origins of diversity, through elaboration of a previous conceptual model. We posit that independent evolution of the sexes may play a facilitating role in diversification, because niches favoured by natural selection are often sex specific. At the same time, the cross-sex genetic correlations, r_mf, which may facilitate tracking a shared peak, acts as a constraint when favoured niches are sex specific. Moreover, we suggest that the existence of sex-specific niches may open a greater array of adaptive phenotype space for a diversifying lineage to explore. This novel view of independent evolution of the sexes raises open empirical questions such as; has relaxation of constraints on male and female evolution played a central role in facilitating diversification? To what degree does the presence of two sexes, and the prevalence and extent of phenotypic differences between them, change the dynamics of deep time diversification compared to the rest of the tree of life, which does not display such pervasive and striking within-species diversity?

Sexual selection favors traits that confer advantages in the competition for mates. In many cases, such traits are costly to produce and maintain, as the costs help to enforce the honesty of these signals and cues. Some evolutionary models predict that sexual selection also produces costs at the population level, which could limit the ability of populations to adapt to changing conditions and thus increase the risk of extinction. Other models, however, suggest that sexual selection should enhance the removal of deleterious mutations and increase rates of adaptation, thus protecting populations against extinction. Previous attempts to test the conflicting predictions produced by these models have been limited to extant species and thus have relied on indirect proxies for species extinction such as population decline or conservation status. Dr Hunt exploits the uniquely informative fossil record of cytheroid ostracodes, (small, bivalved crustaceans with sexually dimorphic carapaces), to provide the first test of how sexual selection relates to actual species extinction. He shows that species with more pronounced sexual dimorphism, indicating the highest levels of male investment in reproduction, had estimated extinction rates ten times higher than lowest-investment species. These results indicate that sexual selection can be a substantial risk factor for extinction.

Why do many animals possess exaggerated sexual ornaments, why are some ornaments more exaggerated than others, and how can one identify sexually-selected traits in fossils of extinct animals? I will introduce the mathematics underlying two influential ideas from evolutionary biology: handicaps and indexes. Handicaps are exaggerated signals that are kept honest by quality-dependent costs paid by signallers, such that high-quality signallers benefit from producing exaggerated signals. Indexes are cost-free (and often subtle) signals, which are instead kept honest by the physical impossibility of dishonesty. Recent theoretical work has concluded that rather than being distinct concepts, handicaps and indexes are opposite ends of the same continuum. This theory makes predictions for the allometric slopes that are predicted to evolve for sexual signals, making it relevant to empirical studies of extinct or extant taxa that use allometric relationships to infer the functional relevance of traits.

The fossil record offers opportunities to assess long term or repeated evolutionary phenomena that are otherwise impossible for living taxa. However, this is not without the considerable issues of the incompleteness of the fossils record and the problems associated with extracting data from it to tackle macroevolutionary questions. In addition to the often small sample sizes available (for single species or across lineages), most specimens will be of uncertain sex and perhaps uncertain age. Samples may be highly biased or exclusively composed of a single sex without our knowledge. Large samples where they do exist may cover a very broad range of populations that varied and time and space. The morphological species concept can make it difficult to even identify putative members of the same species, comparisons to extant taxa may be difficult, and critical traits such as crests or horns may be absent in large numbers of animals. However, awareness of these issues allows for creation and testing of hypotheses that account for the limited data, or at least interpreted in the light of such difficulties. There are intriguing and unexplored datasets that can be collected and analysed and this will require the expertise of both palaeontologists and neontologists.

Charles Darwin may have invented the concept of sexual selection even before he conceived of natural selection. His original purpose was to explain the striking dimorphisms between males and females of a species, which could not be explained by natural selection and therefore posed a potential weakness to that theory. Darwin saw that these structures, usually possessed by the male, were used to attract mates and (or) to repel rivals for mates. There is no question of the centrality of sexual dimorphism (and not simply sexual differences or size differences or allometric differences) to Darwin’s sexual selection: in The Descent of Man he surveys all the animal phyla (over 300 examples) for sexually dimorphic features, and when he finds none in a group he consistently declares it of no interest to his theory.  

Without sexually dimorphic structures it is impossible to identify sexual selection in extinct animals. Taxonomic analogies of “bizarre structures” are weak but may be plausible if specific features are keyed to diagnostic functions. Species recognition, a common but understudied syndrome of living animals, is a better explanation for non-dimorphic elaborate structures, even if there are slight differences in expression between putative males and females in extinct taxa, because these are often the result of simple size differences between the sexes that are not related to sexual selection. “Mutual sexual selection” is an invalid concept. Darwin recognized humans as the only species in which each sex has selected (different) features in the other; this explains his book’s title.

The ‘positive allometry hypothesis’ predicts that ornaments and weapons of sexual selection scale steeply when variation in trait size is compared with variation in overall body size. Intuitive and striking, this idea has been explored in hundreds of animal species and sparked controversy in paleobiology over the function of exaggerated structures in dinosaurs and other extinct lineages. Recently, however, the validity of this hypothesis has been challenged.

Mr O’Brien will address this controversy in two ways. First, he suggest the positive allometry hypothesis be applied only to morphological traits that function as visual signals of body size. Second, because steep scaling slopes make traits better signals than other body parts, he proposes that tests of the positive allometry hypothesis compare the steepness of the scaling relationships of focal, putative signal traits, to those of other body parts within the same organism.

He will provide data for a suite of extreme structures and show that steep scaling relationships are common when structures function as signals, but not for comparably extreme structures that function in other contexts. He will discuss these results in the context of animal signalling and sexual selection, and conclude that patterns of static scaling offer powerful insight into the evolution and function of disproportionately large, or extreme, animal structures. Finally, using data from a ceratopsid dinosaur and a pterosaur, he will show how our revised test can be applied to fossil assemblages, making this an exciting and powerful method for gleaning insight into the function of structures in extinct taxa.