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Sexual selection: patterns in the history of life

Scientific meeting

Starts:

May
092018

09:00

Ends:

May
102018

17:00

Location

Kavli Royal Society Centre, Chicheley Hall, Newport Pagnell, Buckinghamshire, MK16 9JJ

Overview

Theo Murphy international scientific meeting organised by Dr Rob Knell, Dr Dave Hone and Professor Doug Emlen

Peacock Spider, copyright: Jurgen Otto

Sexual selection is potentially an important driver of macroevolutionary processes like speciation and extinction, but this has rarely been tested using the fossil record. This meeting will bring biologists and palaeontologists together to discuss sexual selection’s role in macroevolution, how to detect it in extinct animals and how to measure its influence on the history of life across geological time.

The speaker abstracts and biographies are available below. Recorded audio of the presentation will be available on this page after the meeting has taken place. 

Enquiries: Contact the Scientific Programmes team.

Event organisers

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Schedule of talks

09 May

09:00-12:15

Session 1

8 talks Show detail Hide detail

Chairs

Professor Mike Ritchie, University of St Andrews, UK

09:05-09:30 Males exist. Does it matter?

Professor Hanna Kokko, University of Zurich, Switzerland

Abstract

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).

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09:30-09:45 Discussion

09:45-10:15 Speciation by sexual selection - the role of ecological effects on sexual communication

Dr Martine Maan, University of Groningen, The Netherlands

Abstract

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.

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10:15-10:30 Discussion

11:00-11:30 Sex biased selection and diversification

Professor Locke Rowe, University of Toronto, Canada

Abstract

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, rmf, 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?

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11:30-11:45 Discussion

11:45-12:15 Does sexual selection increase extinction risk? A test using fossil ostracodes

Dr Gene Hunt, National Museum of Natural History, Smithsonian Institution, USA

Abstract

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.

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12:15-12:30 Discussion

12:30-13:30

Lunch

13:30-17:00

Session 2

8 talks Show detail Hide detail

Chairs

Dr Darren Naish, University of Southampton, UK

13:30-14:00 Sexual selection, allometry and the cost of honest signalling

Dr Luke Holman, University of Melbourne, Australia

Abstract

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.

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14:00-14:15 Discussion

14:15-14:45 Problems and potential solutions associated with identifying sexually selected structures in the fossil record

Dr Dave Hone, Queen Mary University of London, UK

Abstract

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.

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14:45-15:00 Discussion

15:30-16:00 Definitions and diagnoses in the fossil record: sexual selection vs species recognition and other processes

Professor Kevin Padian, University of California, Berkeley, USA

Abstract

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.

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16:00-16:15 Discussion

16:15-16:45 The evolution of extreme structures: inferring function from pattern

Mr Devin O'Brien, University of Montana, USA

Abstract

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.

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16:45-17:00 Discussion

10 May

09:00-12:30

Session 3

8 talks Show detail Hide detail

Chairs

Professor Doug Emlen, University of Montana, USA

09:00-09:30 Sexually dimorphic structures in mammals: can we use them to draw inference about past environments?

Professor Christine Janis, University of Bristol, UK

Abstract

The pattern of sexual dimorphism in ungulate (hoofed) mammals in relation to habitat preference was established by Peter Jarman in the early 1970s. He proposed five categories of ecomorphology within African antelopes that related to body size, size dimorphism, and dimorphism in horns. These ecomorphologies were correlated with differences in reproductive behaviour, which in turn were correlated with habitats ranging from closed forest to open grasslands. Thus the distribution of such ecomorphologies within fossil communities may provide information about the habitat independent of other palaeoenvironmental proxies. While sexual dimorphism in body size is difficult to determine in fossils, absolute body size and patterns of the possession of horns (or other types of cranial appendages) can be observed. The pattern of acquisition of cranial appendages and changes in lineages over time can provide information about habitat changes both within and between geographic areas. Cranial appendages first appeared in artiodactyls in the mid Cenozoic at a time when more open habitats started to spread in the higher latitudes: but patterns of acquisition and distribution of dimorphic ecomorphologies differ between ungulates in North America and the Old World, implying earlier and more significant aridity on the North American continent (an implication now confirmed by other proxies). Patterns of horn dimorphism in African bovids may serve to illuminate habitat change over time on that continent.

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09:30-09:45 Discussion

09:45-10:15 Sexual selection on colour signals: mechanisms and diversity

Associate Professor Devi Stuart-Fox, University of Melbourne, Australia

Abstract

Sexual dichromatism, the difference between the sexes in coloration, is one of the most widely used indices of sexual selection in macroevolutionary studies. These studies have revealed evolutionary drivers of the strength of sexual selection, patterns of evolutionary losses and gains of sexual dichromatism, and associations between sexual dichromatism and rates of diversification (including speciation and/or extinction). But how robust is sexual dichromatism as a measure of sexual selection? What are the pitfalls and strengths of this measure? Measures of sexual dichromatism vary widely, limiting our ability to directly compare results between studies, and most do not account for receiver vision. This is important, both because animal colour vision varies substantially, and because the relationship between coloration and signal salience is likely non-linear. Colour is also produced by a variety of mechanisms, for example, pigmentary and structural. This has important implications for costs and constraints on colour variation, and therefore it is utility as a measure of sexual selection. Mechanisms of colour production also have implications for our ability to measure or reconstruct coloration of preserved and fossil specimens. Sexual dichromatism is a useful measure of the strength of sexual selection to identify patterns in the history of life, but coloration is multifaceted and must be understood in its biological context.

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10:15-10:30 Discussion

11:00-11:30 Variation rates as an indication of sociosexual display in horned dinosaurs, and other ornithischians

Dr Caleb Brown, Royal Tyrrell Museum, Canada

Abstract

Phenotypic variation is the basic material upon which selection acts, and as such quantifying this variation is an important aspect of evolutionary biology. Specifically, research on a diverse array of living animals has documented higher rates of morphological variation in sociosexual display structures, than those under natural selection.

Many dinosaur species, particularly ornithischians, exhibit ‘exaggerated’ skeletal structures that lack obvious mechanical functions and have been hypothesized to have function is sexual and social display. These are often manifested as outgrowths/hypertrophy of the skull roof, including the solid and hollow crests of Hadrosauridae, the horns and frills of Ceratopsia, and the thickened domes of Pachycephalosauria. For dinosaur palaeobiology, however, intraspecific variation is often regarded as merely an obstacle to robust taxonomy.

Here morphological variation was quantified (using coefficient of variation) for the well-sampled species of horned dinosaur Centrosaurus apertus, as well as complementary dataset of the horned dinosaurs Anchiceratops, Chasmosaurus, Protoceratops, and the duck-billed dinosaurs Lambeosaurus, and Corythosaurus. 

Levels of variation for the putative ornamentation structures (e.g. frills, horns, crests) are significantly higher (~2-3 times) than those for the remainder of the skull. These results are consistent with, and often statistically indistinguishable from, the known sexual displays of a comprehensive dataset of extant amniotes analogues (including mammals, birds, and squamates).

When combined with previous research suggesting these same structures in ornithischians are ontogenetically delayed, positively allometric, rapidly evolving, and highly species-specific, these data provide further support to the hypothesis that sociosexual selection was the evolutionary driver of these ‘exaggerated’ structures. 

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11:30-11:45 Discussion

11:45-12:15 Sexual selection, adaptation and extinction: lessons from experimental evolution

Professor Jacek Radwan, Adam Mickiewicz University in Poznan, Poland

Abstract

Failure of populations to adapt to sudden environmental changes may lead to extinction. Sexual selection can have multiple, and often opposing, influences on extinction probability. Whether the net outcome of these influences is increased, or decreased, extinction risk is an open empirical question. Professor Radwan will demonstrate how experimental evolution can be used to address this question, focusing on his own work utilising mite species with males differing in expression of a costly sexually selected trait.

Show speakers

12:15-12:30 Discussion

12:30-13:30

Lunch

13:30-17:00

Session 4

7 talks Show detail Hide detail

Chairs

Dr Rob Knell, Queen Mary University of London, UK

13:30-14:00 Quantifying the evolution of theropod cranial ornaments

Dr Terry Gates, North Carolina Museum of Natural Sciences, USA

Abstract

Ornamental signalling structures function to convey messages about an individual organism’s defensive capability, physiology and genetic identity. Across evolutionary time these ornamental structures can be subject to directional selection that increases their size and/or complexity.  These same forces may also act on other aspects of an organism’s physiology or morphology, such that ornamental and non-ornamental traits evolve in tandem. Work from the Gates lab has shown that non-avian theropod species with bony cranial ornaments evolved large body size faster and in most cases topped a greater maximum size than those non-avian species that lacked such bony structures. Terry follows this work by exploring the link between body size and osteological cranial ornaments in galliform birds with two important results. First, bony cranial ornaments in galliforms also characterize species of the largest body size. Ornstein-Uhlenbeck modelling suggests that species of the largest body size tend to have the most ornamented crania when osteological and soft tissue ornaments are taken together. The group’s data also indicate that habitat (coded as a discrete character) of modern Galliformes plays a role in the presence or absence of cranial ornamentation, providing evolutionary biologists with a possible tool for interpreting the ecology of extinct non-avian theropods. The use of quantitative analyses is essential to understanding the effect of ornaments on organismal evolution. Practitioners of these methods should interpret their results in light of null models based on sexual selection or species recognition theory, which can vary dramatically depending on the conditions of selection.

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14:00-14:15 Discussion

14:15-14:45 Weapons versus signals in sexual systems and their potential impact on macroevolution

Dr Erin McCullough, University of Western Australia, Australia

Abstract

Sexual selection researchers often start their papers in the same way – by highlighting the diversity of conspicuous secondary sexual traits. But despite decades of research interest, Dr McCullough would argue that much of this diversity actually remains poorly understood. In this talk, Dr McCullough will discuss two issues hampering our understanding of sexual selection and how it drives the diversity of sexually selected traits. First, the focus of sexual selection research is skewed towards female mate choice. The unfortunate consequence of this bias is that the terms ‘sexual selection’ and ‘mate choice’ are now often used interchangeably, and the term ‘ornament’ is often used to refer generally to all types of sexually selected traits. Dr McCullough thinks that this imprecise terminology is problematic, and she will explain why the distinction between male-male competition and female choice is important. Second, it’s often assumed that sexually selected traits are always signals. Although many sexually selected traits certainly are signals (either to attract females or to threaten rivals), the weapons that are used directly during male-male fights may sometimes only function as tools. Interspecific differences in the relative importance of fighting versus signalling may have important implications for how these structures scale with body size, and when and why some weapons become exaggerated. In order to fully understand the diversity of sexually selected traits, we need to recognize that ornaments are different from weapons, and that weapons are different from signals.

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14:45-15:00 Discussion

15:30-16:00 Adaptation, extinction and environmental change in the fossil record

Professor Erin Saupe, University of Oxford, UK

Abstract

The ability of species to adapt to differing rates of environmental change remains largely unknown. The fossil record can elucidate these dynamics by directly examining the rate at which species evolve their tolerances, or abiotic niches, in response to climatic perturbations over long time scales. Sexual selection is hypothesised to have an effect on rates of niche evolution under some evolutionary models. Long-term evolutionary dynamics derived from the fossil record can inform on any potential relationship between sexual selection and rates of niche evolution. For example, does sexual selection result in lower rates of niche adaptation in comparison to lineages subject solely to natural selection, and does this in turn increase their risk of extinction? Do rates of niche adaption differ in males and females that have been sexually selected? Professor Saupe will demonstrate how these questions can be tackled using the last three million years of niche evolution in marine molluscs from the Western Atlantic. She will additionally discuss the value of the fossil record for quantifying rates of adaption in morphological traits putatively linked to sexual selection, and for testing the influence of sexual selection on rates of speciation and extinction over geological time scales.

Show speakers

16:00-16:15 Discussion

16:15-17:00 Panel discussion: overview (future directions)

Sexual selection: patterns in the history of life

9 - 10 May 2018

Kavli Royal Society Centre, Chicheley Hall Newport Pagnell Buckinghamshire MK16 9JJ
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