TRADE-OFFS AMONG SEXUAL BEHAVIOURS AND TRAITS

When it comes to sex, you can’t have it all. Animals must balance their investment in behaviours and traits important before and after mating. My lab tries to understand how animals balance the competing demands of sex. We address this question experimentally in the lab using halfbeak fishes as a model. Halfbeaks are small, live-bearing freshwater fish from Southeast Asia that are easy to keep and breed in the lab. These fish show overt competitive behaviours, display sexual ornaments and multiple mating is common, making them an ideal model for assessing trade-offs among sexually selected traits. 

 

 

THE EVOLUTION REPRODUCTIVE BEHAVIOURS

Females mate with multiple males in most animal species, which has important evolutionary consequences. We are using phylogenetic comparative analyses to explore how variation in female promiscuity influences the evolution of male sexual behaviours and traits. This work focuses on sharks and rays, bony fish, social insects, marine mammals, and mammals generally. We explore how co-evolutionary dynamics between males and females influence the evolution of testes, sperm, genitals and female remating rates and assess trade-offs at the macroevolutionary scale.

 

SPERM BEHAVIOUR AND EVOLUTION

Competition and choice for reproductive opportunities doesn't end at mating. Our lab focuses on how sperm compeition shapes sperm behaviour, how sperm respond to chemoattractants released by the eggs (or surrounding cells), and how sperm-female interactions influence sperm behaviour. This work spans the animal tree of life, including work on marine invertebrates, fish and humans. 

 

THE EVOLUTION OF ANIMAL COLOURATION

Animals display an enormous variation in colouration and patterns, which is shaped by both natural and sexual selection. Our lab examines both of these selective forces to gain a better understanding of why animals look the way they do. We combine phylogenetic comparative studies with experimental approahces using our lab populations of bamboo sharks and halfbeak fish. 

 

EDITORIAL POSITIONS

2014-2018: Editor for Behavioral Ecology 
2011-2015: Board of Reviewing Editors for Journal of Evolutionary Biology

 

RECENT PUBLICATIONS

For a complete list of publications plase see my Google Scholar page.

 

Some recent highlights: 

In a new paper published in Nature Ecology and Evolution, Ariel Kahrl, Rhonda Snook and I show that females supercharge sperm evolution in animals. This paper was a real labour of love - including sperm data from 3,233 species from 21 animal phyla! 

 

Do animals avoid inbreedign when given the chance? In a new paper published in Nature Ecology and Evolution, Raissa de Boer and Regina Vega-Trejo lead a meta-analysis spanning 40 years of resaerch. The upshot is that there is very little evidence that animals avoid inbreeding in experimental settings.  

 

Charel Reuland leads an multi-national team as he publishes the third chapter from his PhD thesis in Cells. It turns out sperm evolve slower than sexual weapons like horns and antlers.

 

Charel Reuland looks at how social dominace influences ejaculate traits in halfbeaks as he publishes the second chapter from his PhD thesis in Behavioral Ecology!

 

Microscopic mate choice! In a paper published in Proceedings B, we show that human eggs are better at attracting sperm from some males than others. While no where near definitive, these results suggest that mate choice might occur at the gametic level in humans. This paper has been downloaded more than 50,000 times so far and was featured in 126 news articles in 21 languages! 

Some earlier highlights: 

In a new paper published in Nature Communications, Leigh Simmons and I show that female genitalia evolve rapidly in dung beetles - evolving even faster than male genitalia!

Leigh Simmons, Stefan Lüpold and I explore the world of evolutionary trade-offs among sexual traits in animals in a new paper published in TREE.

 

Cody Dey leads a multinational team to evaluate why fish evolve complex cooperative behaviours in an article published in Nature Ecology and Evolution.

I urval från Stockholms universitets publikationsdatabas

• Behavioral Variation in the Pygmy Halfbeak Dermogenys collettei

  2021. Alessandro Devigili (et al.). Frontiers in Ecology and Evolution 9

  Artikel

  Variation in biotic and abiotic factors among populations affects individual behaviors by transforming the social landscape and shaping mating systems. Consequently, describing behaviors in natural populations requires consideration of the biological and physical factors that different individuals face. Here, we examined variation in socio-sexual and locomotor behaviors in a small, livebearing, freshwater fish, the pygmy halfbeak Dermogenys collettei, across natural populations in Singapore. The pygmy halfbeak is a surface feeding fish that spends most of the time near the water surface, making it ideal for non-invasive behavioral observations. We compared behaviors between sexes among 26 shoals while simultaneously accounting for environmental variation. We demonstrated that sexual interactions and locomotor behaviors differed among shoals with varying levels of canopy cover and water flow. Specifically, in areas with greater canopy cover, sexual interactions decreased, whereas time spent in a stationary position increased. Sexual interactions were more numerous in still water, where fish spent less time swimming. Variation in the expression of socio-sexual and locomotor behaviors were not associated with differences in the amount of aquatic vegetation, water depth or halfbeak shoal size. Agonistic interactions were robust to environmental effects, showing little variation among environments. However, there were strong sex effects, with males performing more agonistic behaviors and spending less time in a stationary position compared to females, regardless of the environment. Moreover, sexual interactions, measured as actively performed by males and passively received by females, were on average more frequent in males than in females. Our findings help us explore the proximal causes of intraspecific behavioral variation and suggest that fundamental information on socio-sexual behaviors from wild populations can lead to a better understanding of how sexual selection operates when the strength of natural selection varies across environments.

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• Male-male behavioral interactions drive social-dominance-mediated differences in ejaculate traits

  2021. Charel Reuland (et al.). Behavioral Ecology 32 (1), 168-177

  Artikel

  Higher social status is expected to result in fitness benefits as it secures access to potential mates. In promiscuous species, male reproductive success is also determined by an individual's ability to compete for fertilization after mating by producing high-quality ejaculates. However, the complex relationship between a male's investment in social status and ejaculates remains unclear. Here, we examine how male social status influences ejaculate quality under a range of social contexts in the pygmy halfbeak Dermogenys collettei, a small, group-living, internally fertilizing freshwater fish. We show that male social status influences ejaculate traits, both in the presence and absence of females. Dominant males produced faster swimming and more viable sperm, two key determinants of ejaculate quality, but only under conditions with frequent male-male behavioral interactions. When male-male interactions were experimentally reduced through the addition of a refuge, differences in ejaculate traits of dominant and subordinate males disappeared. Furthermore, dominant males were in a better condition, growing faster, and possessing larger livers, highlighting a possible condition dependence of competitive traits. Contrary to expectations, female presence or absence did not affect sperm swimming speed or testes mass. Together, these results suggest a positive relationship between social status and ejaculate quality in halfbeaks and highlight that the strength of behavioral interactions between males is a key driver of social-status-dependent differences in ejaculate traits.

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• Chemical signals from eggs facilitate cryptic female choice in humans

  2020. John L. Fitzpatrick (et al.). Proceedings of the Royal Society of London. Biological Sciences 287 (1928)

  Artikel

  Mate choice can continue after mating via chemical communication between the female reproductive system and sperm. While there is a growing appreciation that females can bias sperm use and paternity by exerting cryptic female choice for preferred males, we know surprisingly little about the mechanisms underlying these post-mating choices. In particular, whether chemical signals released from eggs (chemoattractants) allow females to exert cryptic female choice to favour sperm from specific males remains an open question, particularly in species (including humans) where adults exercise pre-mating mate choice. Here, we adapt a classic dichotomous mate choice assay to the microscopic scale to assess gamete-mediated mate choice in humans. We examined how sperm respond to follicular fluid, a source of human sperm chemoattractants, from either their partner or a non-partner female when experiencing a simultaneous or non-simultaneous choice between follicular fluids. We report robust evidence under these two distinct experimental conditions that follicular fluid from different females consistently and differentially attracts sperm from specific males. This chemoattractant-moderated choice of sperm offers eggs an avenue to exercise independent mate preference. Indeed, gamete-mediated mate choice did not reinforce pre-mating human mate choice decisions. Our results demonstrate that chemoattractants facilitate gamete-mediated mate choice in humans, which offers females the opportunity to exert cryptic female choice for sperm from specific males.

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• Contrasting female mate preferences for red coloration in a fish

  2020. Charel Reuland (et al.). Current Zoology 66 (4), 425-433

  Artikel

  Understanding how animals select their mates requires knowing the factors that shape mate preferences. Recent theoretical and empirical considerations suggest that female mating status can influence the degree to which a female engages in mate choice, with virgin females predicted to be less choosy than mated females. In this study, we investigated mate choice in both virgin and mated females in the pygmy halfbeak Dermogenys collettei. Halfbeaks are small, live-bearing, internally fertilizing freshwater fish that live in mixed-sex groups where females have ample opportunity to engage in mate choice. Using a dichotomous choice assay, we quantified and contrasted in virgin and mated females mate preferences for differences in male body size, beak size, and area of yellow and red coloration. We also examined how mating status influenced the amount of time a female associated with the first male encountered and the relative amount of time a female associated with each male. We demonstrate that mate preferences of female halfbeaks are driven primarily by the size of red coloration present on males. Females showed contrasting preferences based on mating status, with virgin females preferentially associating with drab males whereas mated females preferentially associate with males possessing large areas of red. Contrary to expectations, female mating status did not influence how females associate with the first males encountered or how females biased their association time among males. Although the precise drivers of these effects need further studying, our finding highlights a possible explanation for how variation in male ornamentation can be maintained.

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• How sperm competition shapes the evolution of testes and sperm

  2020. Stefan Lüpold (et al.). Philosophical Transactions of the Royal Society of London. Biological Sciences 375 (1813)

  Artikel

  Females of many species mate with multiple males, thereby inciting competition among ejaculates from rival males for fertilization. In response to increasing sperm competition, males are predicted to enhance their investment in sperm production. This prediction is so widespread that testes size (correcting for body size) is commonly used as a proxy of sperm competition, even in the absence of any other information about a species' reproductive behaviour. By contrast, a debate about whether sperm competition selects for smaller or larger sperm has persisted for nearly three decades, with empirical studies demonstrating every possible response. Here, we synthesize nearly 40 years of sperm competition research in a meta-analytical framework to determine how the evolution of sperm number (i.e. testes size) and sperm size (i.e. sperm head, midpiece, flagellum and total length) is influenced by varying levels of sperm competition across species. Our findings support the long-held assumption that higher levels of sperm competition are associated with relatively larger testes. We also find clear evidence that sperm competition is associated with increases in all components of sperm length. We discuss these results in the context of different theoretical predictions and general patterns in the breeding biology and selective environment of sperm. This article is part of the theme issue 'Fifty years of sperm competition'.

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• Male mate choice for large gravid spots in a livebearing fish

  2020. Hannah J. P. Ogden (et al.). Behavioral Ecology 31 (1), 63-72

  Artikel

  Male mate choice occurs in a wide range of species, and males can increase their reproductive success by distinguishing between females based on their fecundity (e.g., large body size) or their expected sperm competition risk (e.g., virgins). However, patterns of male mate choice could be mitigated by variation in female physiological receptivity, as males can benefit by directing their mating efforts toward females that are at a point in their reproductive cycle when fertilization probability is highest. Here, we perform three experiments to assess whether male mate choice is influenced by cues of female physiological receptivity, fecundity, or sperm competition risk in the pygmy halfbeak (Dermogenys collettei), a small livebearing fish. Female halfbeaks possess a gravid spot-an orange abdominal marking that is caused by pigmentation of the females' skin and variation in embryo development and pigmentation during pregnancy. We show that gravid spot size increases toward parturition and is largest right before giving birth, independent of abdominal width or body size. Males consistently chose females with large gravid spots over females with small gravid spots. In contrast, males did not prefer larger females over smaller females or virgin females over mated females. As female halfbeaks store sperm prior to fertilizations, we suggest that males use the size of the gravid spot as a cue to direct their mating efforts to those females where the chance of fertilization is highest.

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• Repeated evidence that the accelerated evolution of sperm is associated with their fertilization function

  2020. John L. Fitzpatrick, C. Daisy Bridge, Rhonda R. Snook. Proceedings of the Royal Society of London. Biological Sciences 287 (1932)

  Artikel

  Spermatozoa are the most morphologically diverse cell type, leading to the widespread assumption that they evolve rapidly. However, there is no direct evidence that sperm evolve faster than other male traits. Such a test requires comparing male traits that operate in the same selective environment, ideally produced from the same tissue, yet vary in function. Here, we examine rates of phenotypic evolution in sperm morphology using two insect groups where males produce fertile and non-fertile sperm types (Drosophila species from the obscura group and a subset of Lepidoptera species), where these constraints are solved. Moreover, in Drosophila we test the relationship between rates of sperm evolution and the link with the putative selective pressures of fertilization function and postcopulatory sexual selection exerted by female reproductive organs. We find repeated evolutionary patterns across these insect groups-lengths of fertile sperm evolve faster than non-fertile sperm. In Drosophila, fertile sperm length evolved faster than body size, but at the same rate as female reproductive organ length. We also compare rates of evolution of different sperm components, showing that head length evolves faster in fertile sperm while flagellum length evolves faster in non-fertile sperm. Our study provides direct evidence that sperm length evolves more rapidly in fertile sperm, probably because of their functional role in securing male fertility and in response to selection imposed by female reproductive organs.

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• Sperm competition and fertilization mode in fishes

  2020. John L. Fitzpatrick. Philosophical Transactions of the Royal Society of London. Biological Sciences 375 (1813)

  Artikel

  Sperm competition is a powerful selective force that has shaped sexual traits throughout animal evolution. Yet, how fertilization mode (i.e. external versus internal fertilization) influences the scope and potential for sperm competition to act on ejaculates remains unclear. Here, I examine how fertilization mode shapes ejaculatory responses to sperm competition in fishes, a diverse group that constitute the majority of vertebrate biological diversity. Fishes are an ideal group for this examination because they exhibit a wide range of reproductive behaviours and an unparalleled number of transitions in fertilization mode compared to any other vertebrate group. Drawing on data from cartilaginous and bony fishes, I first show that rates of multiple paternity are higher in internally than externally fertilizing fishes, contrary to the prevailing expectation. I then summarize how sperm competition acts on sperm number and quality in internally and externally fertilizing fishes, highlighting where theoretical predictions differ between these groups. Differences in how ejaculates respond to sperm competition between fertilization modes are most apparent when considering sperm size and swimming performance. Clarifying how fertilization mode influences evolutionary responses in ejaculates will inform our understanding of ejaculate evolution across the animal tree of life. This article is part of the theme issue 'Fifty years of sperm competition'.

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