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Overview

Theo Murphy meeting organised by Professor Vincent Savolainen, Professor Sergey Gavrilets and Professor Nathan Bailey

Homosexuality is common in animals and humans, but the biological foundations of such behaviour are unknown. Instead, as offspring are not produced, it is considered a Darwinian paradox. This meeting will confront genetic mechanisms and socio-evolutionary models underlying sexual orientation, in light of recent genomic findings, and with the aim to provide a modern, science-led synthesis on this topic.

Poster session

There will be an in-person poster session on Monday 27 March at the meeting venue. If you would like to apply to present a poster please submit your proposed title, abstract (not more than 200 words and in third person), author list, name of the proposed presenter and institution to the Scientific Programmes team no later than Friday 10 March 2023.

Please include the text 'Poster abstract submission - Genetics and evolution of sexual orientation' in the email subject line. Please note that posters are selected at the scientific organisers' discretion.

Attending this event

This meeting is intended for researchers in relevant fields. This will be a residential meeting held at Moor Hall, Cookham, Maidenhead, Berkshire, SL6 9QH.

  • Free to attend
  • Limited places, advance registration essential
  • This is an in-person meeting only
  • Meals during the meeting can be paid for through Eventbrite (lunches on both days of the meeting and dinner on the first night)
  • Participants will need to book their own accommodation with Moor Hall.

Enquiries: contact the Scientific Programmes team

Organisers

Schedule


Chair

09:00-09:05
Welcome by lead organiser
09:05-09:30
The evolutionary history of homosexual behaviour in female Japanese macaques

Abstract

Multiple studies indicate that female homosexual behaviour in Japanese macaques (Macaca fuscata) is not an adaptation and serves no fitness enhancing function. How do non-adaptive behaviours, like this, evolve? To account for the existence of such a trait, Professor Vasey proposed a four-stage model for the evolutionary history of female mounting in Japanese macaques. The model holds that: (i) play mounting among immature male Japanese macaques evolved to solicit the attention of play partners and prolong interactions; (ii) adult females exploited this evolutionary “loophole” for their own adaptive ends by using female-male mounting to focus their male consort partners’ attention and expedite male-female mounting in a context of high female-female competition for male mates; (iii) females then evolved the capacity to derive sexual reward from female-male mounting via genital stimulation; and, (iv) next, female-female mounting evolved as a neutral by-product of selection for female-male mounting and because females’ could obtain sexual reward during mounts. Once this capacity evolved, females sometimes chose female sexual partners despite the presence of sexually motivated males. The author will discuss research aimed at testing this model which has been conducted over the past two decades.

Speakers

09:30-09:45
Discussion
09:45-10:15
Same-sex sociosexual behaviour is widespread and heritable in male rhesus macaques

Abstract

Historically, same-sex sociosexual behaviour (SSB) has been labelled a ‘Darwinian paradox’, due to the belief that individuals who engage in SSB will have reduced fitness and be selected against. The authors collected detailed observations across three years of social and mounting behaviour of 236 male semi-wild rhesus macaques, which they combined with a pedigree dating back to 1938 to show that SSB was both repeatable and heritable, while age and group structure explained SSB only marginally. Furthermore, they found no fitness cost to SSB, but show instead that the behaviour mediated coalitionary partnerships associated with likely fitness benefits. Their results lay to rest the Darwinian paradox of SSB by showing how it can evolve, with implications for a more inclusive understanding of the behaviour in nature and society.

Vincent Savolainen, Jackson Clive, and Ewan Flintham

Georgina Mace Centre for the Living Planet, Department of Life Sciences, Imperial College London

Speakers

10:15-10:30
Discussion
10:30-11:00
Break
11:00-11:30
Some phenotypic considerations for an evolutionary theory of sexual orientation

Abstract

Sexual orientation is the relative sexual desire for male or female sex partners. Heterosexual orientation is evolutionarily adaptive because it facilitates reproduction. Yet in the contemporary west, appreciable minorities of men and women report that their orientation is not entirely heterosexual. A review of contemporary western studies estimated the percentages of mostly or entirely homosexual-attracted men and women to be 2.1% and 1.1%, respectively (Bailey et al., 2016). Research from some traditional societies is consistent with the figure for men. (Women have been studied less often in those societies.) Most phenotypic research on sexual orientation has focused on differences between homosexual and heterosexual persons, ignoring bisexuals. This is especially true for men, among whom bisexuality is rarer. 

Male and female sexual orientation share at least one important and strong correlate: degree of gender nonconformity, which is greater for nonheterosexual individuals. This correlate begins in childhood and is moderately persistent into adulthood. 

An important difference between male and female sexual orientation concerns sexual arousal patterns, whether measured by self-report, genital response, or neural activation. For men, these patterns are highly predictable from self-reported sexual orientation. Indeed, these arousal patterns arguably define male sexual orientation. Women’s self-reported sexual orientation is only weakly related to their arousal patterns. Among men strong heterosexual arousal motivates search and competition for female mates and enables heterosexual copulation. On average, homosexual men show much stronger sexual arousal to other men than to women. They are the primary evolutionary puzzle of sexual orientation.

Speakers

11:30-11:45
Discussion
11:45-12:15
Plasticity, modularity, and cross-sexual transfer: a nonbinary framework for sexual diversity

Abstract

Same-sex sexual behaviour is widespread in animals. Evolutionary hypotheses address multiple contexts and mechanisms, yet we lack a general framework for sexual diversity that includes same- and different-sex sexual behaviour across contexts. Professor Warkentin suggests we relax two implicit assumptions – binary sexual differentiation and ancestral reproductive heterosexuality – and apply a developmental plasticity framework to examine sexes as alternative morphs within species and sexual behaviour as one of many sex-associated traits. The modularity of sex-associated traits and asynchrony of their development create abundant opportunities for cross-sexual transfer of trait expression, and evolved variation in sex-associated traits suggests such transfer is common. The author posits an ancestral mixture of reproductive and non-reproductive sexual behaviour, due to costs of advertising and discriminating sex and fertility. Recurrent trait expression enables genetic accommodation, through which selection adjusts the form, regulation, and side-effects of the trait. Thus derived, non-conceptive functions of sexual behaviour have evolved, in reproductive and non-reproductive contexts. Positive feedback between diversified functions and expression contexts for sexual behaviour is likely, and both appear prevalent in highly social species, including primates. Cooperative breeding distinguishes humans from other apes. This extreme form of sociality makes reproductive success dependent on alloparental care, increasing the importance of social bonds and value of helping kin and relaxing selection against traits that prevent individual reproduction. The extreme variation in human sexual behaviour evolved in this highly contextual selective environment.

Speakers

12:15-12:30
Discussion
12:30-13:30
Lunch

Chair

13:30-14:00
Genetic and epigenetic models of homosexuality

Abstract

Abstract of the talk will be available soon.

Speakers

14:00-14:15
Discussion
14:15-14:45
Prenatal androgen exposure and human sexual orientation

Abstract

Thousands of experimental studies of non-human mammals have documented the effects of early androgen exposure on later sex-related behaviour. Similar experimental studies of early androgenic influences on human behaviour would not be ethical. Studies of people with genetic syndromes causing unusual androgen exposure prenatally, however, suggest that androgens exert similar influences on human behaviour. For instance, women exposed to high concentrations of androgens prenatally because they have congenital adrenal hyperplasia (CAH) show reduced female-typical and increased male-typical behaviour. Among other outcomes, they are less likely than other women to report being exclusively or almost exclusively heterosexual. Similarly, XY individuals who experience no effective androgen exposure because they have complete androgen insensitivity syndrome (CAIS) almost always report female-typical sexual orientation. These findings suggest that genetic factors that influence androgens or their ability to act during early development contribute to inter-individual variability in human sexual orientation.

Speakers

14:45-15:00
Discussion
15:00-15:30
Break
15:30-16:00
Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behaviour

Abstract

The evolution of same-sex sexual behaviour (SSB) is an enigma because such behaviour cannot directly result in reproduction. Theoretical papers predict that indiscriminate mating is an evolutionary driver of SSB, calling for empirical work to test this hypothesis. Professor Bailey will discuss a study showing that same-sex pairing in termites is maintained not by indiscriminate mating but by behavioural plasticity with accurate sexual discrimination. Female and male termites can express the behaviour of the other sex, which contributes to maintaining pair coordination. Phylogenetic comparative analysis suggests that such behavioural flexibility was inherited from an ancestral lineage. The findings show that SSB can evolve with highly accurate sex discrimination, combined with sex-role plasticity, and they challenge recent arguments for a prominent role of indiscriminate mating behaviour in the evolutionary origin and maintenance of SSB across diverse taxa.

Speakers

16:00-16:15
Discussion
16:15-16:45
What models of sexual arousal can and cannot tell us about the evolution of women's sexual orientation

Abstract

Abstract of the talk will be available soon.

Speakers

16:45-17:00
Discussion
17:00-18:00
Poster session

Chair

09:00-09:30
Genomic evidence consistent with antagonistic pleiotropy may help explain the evolutionary maintenance of same-sex sexual behaviour

Abstract

Human same-sex sexual behaviour (SSB) is heritable, confers no obvious direct reproductive or survival benefit and can divert mating effort from reproductive opportunities. This presents a Darwinian paradox: why has SSB been maintained despite apparent selection against it? Professor Verweij will present results from a study showing that genetic effects associated with SSB may, in individuals who only engage in opposite-sex sexual behaviour (OSB individuals), confer a mating advantage. A genome-wide association study on 477,522 individuals was performed, revealing five loci significantly associated with SSB. In aggregate, these genetic variants accounted for 8 to 25% of individual differences in SSB. Using the results from this study (the genome-wide effect estimates) and results from a genome-wide association study on number of opposite-sex sexual partners in 358,426 individuals, the authors show that, among OSB individuals, genetic effects associated with SSB are associated with having more opposite-sex sexual partners. Simulation analyses suggest that such a mating advantage for alleles associated with SSB could help explain how it has been evolutionarily maintained. Several important caveats will be discussed.

Speakers

09:30-09:45
Discussion
09:45-10:15
Genetically identical twins discordant for sexual orientation: potential reasons for their differences

Abstract

About 75% of genetically identical twins who are homosexual have heterosexual co-twins, and it is largely unknown what causes their difference. However, the majority of past work with such twin pairs was based on self-reports, which can be biased, and how these twins truly differ remained uncertain. The author will summarise research from our lab showing that these twins differ in behavioural, physiological, and anatomical traits linked to sexual orientation: gender-nonconformity, genital arousal, and finger length ratios, respectively. Dr Rieger will then propose a mechanism that explains their different development. About 30% of identical twins develop with separate placentas. Maternal androgens or antibodies could diffuse differently through these placentas, affecting the differentiated development of the twins. The author will also propose a study design to indirectly test this hypothesis.

Speakers

10:15-10:30
Discussion
10:30-11:00
Break
11:00-11:30
Homosexual preference in humans: an evolutionary approach

Abstract

Male homosexual orientation remains a Darwinian paradox, as there is no consensus on its evolutionary (ultimate) determinants. Much work in the previous decades has focused on kin selection, with the conclusion that this explanation alone seems insufficient and cannot explain the origin or the maintenance of same-sex sexual preference in our species. There are several other evolutionary explanations, such as the pleiotropic effects which are now scrutinized, although there is no consensus yet on the nature of the advantageous trait that would be selectively favoured and linked to same-sex attraction. One intriguing feature of homosexual men is their higher male birth rank compared to heterosexual men, best explained by a fraternal birth order effect, and not by a pleiotropic effect on female fertility. However, the effect of male birth order on sexual orientation requires an evolutionary explanation. An overall picture of possible evolutionary determinants of same-sex orientation will be presented. 

Speakers

11:30-11:45
Discussion
11:45-12:15
Large-scale GWAS reveals insights into the genetic architecture of same-sex sexual behaviour

Abstract

Twin studies and other analyses of inheritance of sexual orientation in humans has indicated that same-sex sexual behaviour has a genetic component. Previous searches for the specific genes involved have been underpowered and thus unable to detect genetic signals. Dr Ganna together with a group of scientists perform a genome-wide association study on 493,001 participants from the United States, the United Kingdom, and Sweden to study genes associated with sexual orientation (see the Perspective by Mills). They find multiple loci implicated in same-sex sexual behaviour indicating that, like other behavioural traits, nonheterosexual behaviour is polygenic.

Speakers

12:15-12:30
Discussion
13:30-14:00
Delineating distinct bio-developmental pathways of sexual orientation

Abstract

While prenatal androgens largely mediate sexual behaviour and preferences in non-human animals, the evidence has been mixed when it comes to human sexual orientation and gender expression. In this talk, the authors will present data suggesting that there are multiple biological pathways underlying sexual orientation among humans, and early androgens exposure contributes to the sexual orientation and gender expression of a subset of gay men. The authors approach this research from a translational approach evaluating how the principles gained in studying sexual differentiation of the brain and behaviour in rodent models may apply to humans. As such, Dr Swift-Gallant will also present preliminary work from our rodent models suggesting that alternate mechanisms, such as the gut microbiota, contribute to socio-sexual behaviours and thus may be considered in understanding the biological underpinnings of same-sex sexual orientation in humans.

Speakers

14:00-14:15
Discussion
14:15-14:45
The evolution of same-sex sexual orientation: recent insights from Thailand

Abstract

In Thai culture, same-sex attracted individuals are often considered to be gender-nonbinary and referred to as pheet thii saam, which translates as “third sex/gender.” Males who display androphilia (ie, sexual attraction to adult males) present as either relatively more masculine (ie, gay) or as transfeminine (ie, sao praphet song, which translates as “a second kind of woman”). Females who display gynephilia (ie, sexual attraction to adult females) present as relatively more feminine (ie, lesbian), transmasculine (ie, tom, which has a similar connotation as “tomboy”), or as feminine individuals who are romantically/sexually attracted towards toms (ie, dee). This presentation will detail three recent and ongoing evolutionary studies focusing on same-sex sexual orientation in which these groups of pheet thii saam individuals were compared with heterosexual men and women. Study 1 focused on the numbers of offspring produced by study participants and demonstrates lowered direct reproduction among pheet thii saam relative to their heterosexual counterparts. Study 2 tested the kin selection hypothesis, which posits that same-sex attracted individuals offset their lack of reproduction by allocating kin-directed altruism towards close kin, thus enhancing inclusive fitness. Study 3 tested the balancing selection hypothesis, which posits that the relatives of same-sex attracted individuals exhibit increased reproduction, which could offset same-sex attracted individuals’ lack of reproduction. Together, findings from these studies add to existing empirical work on the evolutionary maintenance of same-sex sexual attraction and help to delineate possible evolutionary differences based on the sex and gender expression of same-sex attracted individuals. 

Speakers

14:45-15:00
Discussion
15:00-15:30
Break
15:30-16:00
Is Sexual Orientation a Spandrel? Reframing genetic-evolutionary understandings of sexual diversity

Abstract

For over 50 years, scientists across multiple disciplines (genetics, anthropology, endocrinology, psychology) have tried - but failed - to nail down the cause of human same-gender sexual expression. Although studies confirm that same-gender sexual behaviour is genetically influenced, the magnitude of this influence appears relatively small, accounting for only 8-25% of the population variance in same-gender sexual behaviour (Ganna et al, 2019). Further complicating matters is the fact that “same-gender sexual expression” does not appear to represent a single phenotype or genotype. Subtypes of same-gender sexuality (early developing, later developing, exclusive, bisexual, fluid, stable) have been documented by anthropologists and psychologists for decades, and recent genetic research suggests that these subtypes may correspond to distinct genetic profiles. Ganna’s (2019) study of the full genomes of over 450,000 individuals made the startling discovery that the genes associated with ever having pursued same-gender sexual behaviour were not the same as the genes associated with degrees of same-gender sexual behaviour. This finding directly contradicts the notion that same-gender and other-gender orientations represent two ends of a single genetic continuum, and suggests scientists may have failed to properly characterize the phenotype of sexual orientation. An additional weakness of prior genetic-evolutionary research on sexual orientation is the inattention to gene-environment interactions, particularly those involving childhood adversity. One of the most robustly documented environmental differences between individuals with same-gender sexual behaviour and individuals without such behaviour is exposure to childhood adversity, including financial hardship, neighbourhood violence, residential instability, physical/sexual abuse, and the unavailability of reliable adult care and protection. From an evolutionary perspective, there is arguably no category of environmental experience as influential on human genetic expression as childhood threat and nurturance. Decades of developmental research has shown that the children’s brains are exquisitely sensitive to such experiences, and decades of evolutionary research has explained why: Early life experiences of threat and nurturance are treated by the developing human brain as “hints” about the types of survival and reproductive challenges a child may face in the future. Accordingly, the fact that same-gender-attracted adults report twice as much childhood adversity as heterosexuals is simply too significant to ignore, especially for scientists grounded in evolutionary models of human development. We need genetically-informed understandings of sexual diversity that adequately capture the full range of human sexual phenotypes and the full range of gene-environment interactions that may shape sexual development. This broadened perspective may lead us to retire the notion of “sexual orientation” altogether, and to question our own culturally-grounded assumptions about sexual “traits.” Gould and Lewontin famously cautioned evolutionary biologists against over-interpreting salient patterns in natural phenomena, noting that some of these patterns are simply “spandrels,” defined as phenotypic by-products of other evolved traits and processes that we fail to observe. In light of this caution, we should actively investigate the possibility that same-gender sexual expression is an “accidental” form of human patterning, whose genetic underpinnings have little to do with either sexual differentiation or sexual reproduction. 

Speakers

16:00-16:15
Discussion
16:15-17:00
Panel discussion/overview