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  • 1.
    Devigili, Alessandro
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Evans, Jonathan P.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Predation shapes sperm performance surfaces in guppies2019In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 286, no 1905, article id 20190869Article in journal (Refereed)
    Abstract [en]

    Sperm velocity is a key determinant of competitive fertilization success in many species. Selection is therefore expected to favour the evolution of faster sperm when the level of sperm competition is high. However, several aspects can determine the direction and strength of selection acting on this key performance trait, including ecological factors that influence both sperm competition and the strength of selection acting on correlated traits that may constrain evolutionary responses in sperm velocity. Here, we determine how a key ecological variable, the level of predation, shapes sperm swimming speed across 18 Trinidadian populations of guppies (Poecilia reticulata). We use performance analysis, a statistical tool akin to the familiar methods of multivariate selection analyses, to determine how the level of predation influences sperm velocity (modelled as a performance trait) when accounting for correlated pre- and postcopulatory traits that are also impacted by predation. We show that predation affects the combination of pre- and postcopulatory traits that ultimately predict sperm performance. Overall, we report evidence for disruptive relationships between sperm performance and combinations of ornaments and sperm morphology, but the specific combinations of traits that predict sperm velocity depended on the level of predation. These analyses underscore the complex nonlinear interrelationships among pre- and postcopulatory traits and the importance of considering ecological factors that may ultimately change the way in which multiple traits interact to determine a trait's performance value. As such, our results are likely to be broadly applicable across systems where selection is influenced by ecological conditions.

  • 2.
    Devigili, Alessandro
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Padova, Italy.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology. University of Western Australia, Australia.
    Gasparini, C.
    Ramnarine, I. W.
    Pilastro, A.
    Evans, J. P.
    Possible glimpses into early speciation: the effect of ovarian fluid on sperm velocity accords with post-copulatory isolation between two guppy populations2018In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 31, no 1, p. 66-74Article in journal (Refereed)
    Abstract [en]

    Identifying mechanisms of reproductive isolation is key to understanding speciation. Among the putative mechanisms underlying reproductive isolation, sperm-female interactions (post-mating-prezygotic barriers) are arguably the hardest to identify, not least because these are likely to operate at the cellular or molecular level. Yet sperm-female interactions offer great potential to prevent the transfer of genetic information between different populations at the initial stages of speciation. Here, we provide a preliminary test for the presence of a putative post-mating-prezygotic barrier operating between three populations of Trinidadian guppies (Poecilia reticulata), an internally fertilizing fish that inhabits streams with different levels of connectivity across Trinidad. We experimentally evaluate the effect of female ovarian fluid on sperm velocity (a predictor of competitive fertilization success) according to whether males and females were from the same (native) or different (foreign) populations. Our results reveal the potential for ovarian fluid to act as a post-mating-prezygotic barrier between two populations from different drainages, but also that the strength of this barrier is different among populations. This result may explain the previous finding that, in some populations, sperm from native males have precedence over foreign sperm, which could eventually lead to reproductive isolation between these populations.

  • 3. Dey, Cody J.
    et al.
    O'Connor, Constance M.
    Wilkinson, Holly
    Shultz, Susanne
    Balshine, Sigal
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology. University of Manchester, UK.
    Direct benefits and evolutionary transitions to complex societies2017In: Nature Ecology and Evolution, ISSN 2397-334X, Vol. 1, no 5, article id 0137Article in journal (Refereed)
    Abstract [en]

    The selective forces that drive the evolution of cooperation have been intensely debated. Evolutionary transitions to cooperative breeding, a complex form of cooperation, have been hypothesized to be linked to low degrees of promiscuity, which increases intragroup relatedness and the indirect (that is, kin selected) benefits of helping. However, ecological factors also promote cooperative breeding, and may be more important than relatedness in some contexts. Identifying the key evolutionary drivers of cooperative breeding therefore requires an integrated assessment of these hypotheses. Here we show, using a phylogenetic framework that explicitly evaluates mating behaviours and ecological factors, that evolutionary transitions to cooperative breeding in cichlid fishes were not associated with social monogamy. Instead, group living, biparental care and diet type directly favoured the evolution of cooperative breeding. Our results suggest that cichlid fishes exhibit an alternative path to the evolution of complex societies compared to other previously studied vertebrates, and these transitions are driven primarily by direct fitness benefits.

  • 4. Fenkes, Miriam
    et al.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Ozolina, Karlina
    Shiels, Holly A.
    Nudds, Robert L.
    Sperm in hot water: direct and indirect thermal challenges interact to impact on brown trout sperm quality2017In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 220, no 14, p. 2513-2520Article in journal (Refereed)
    Abstract [en]

    Climate change alters the thermal habitat of aquatic species on a global scale, generating novel environmental challenges during all life stages, including reproduction. Changes in water temperature profoundly influence the performance of ectothermic aquatic organisms. This is an especially crucial issue for migratory fish, because they traverse multiple environments in order to reproduce. In externally fertilizing migratory fish, gametes are affected by water temperature indirectly, within the reproductive organ in which they are produced during migration, as well as directly, upon release into the surrounding medium at the spawning grounds. Both direct (after release) and indirect (during production) thermal impacts on gamete quality have been investigated, but never in conjunction. Here, we assessed the cumulative influence of temperature on brown trout, Salmo trutta, sperm quality during sperm production (male acclimation temperature) as well as upon release (sperm activation water temperature) on two consecutive dates during the brown trout spawning season. Early in the season, warm acclimation of males reduced their fertilization probability (lower sperm velocity) when compared with cold-acclimated males, especially when the activation water temperature was also increased beyond the thermal optimum (resulting in a lower proportion of motile sperm with lower velocity). Later in the season, sperm quality was unaffected by acclimation temperature and thermal sensitivity of sperm was reduced. These results give novel insights into the complex impacts of climate change on fish sperm, with implications for the reproduction and management of hatchery and wild trout populations in future climate scenarios.

  • 5. Fenkes, Miriam
    et al.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Shiels, Holly A.
    Nudds, Robert L.
    Acclimation temperature changes spermatozoa flagella length relative to head size in brown trout2019In: Biology Open, ISSN 2046-6390, Vol. 8, no 7, article id UNSP bio039461Article in journal (Refereed)
    Abstract [en]

    Temperature is a ubiquitous environmental factor affecting physiological processes of ectotherms. Due to the effects of climate change on global air and water temperatures, predicting the impacts of changes in environmental thermal conditions on ecosystems is becoming increasingly important. This is especially crucial for migratory fish, such as the ecologically and economically vital salmonids, because their complex life histories make them particularly vulnerable. Here, we addressed the question whether temperature affects the morphology of brown trout, Salmo trutta L. spermatozoa. The fertilising ability of spermatozoa is commonly attributed to their morphological dimensions, thus implying direct impacts on the reproductive success of the male producing the cells. We show that absolute lengths of spermatozoa are not affected by temperature, but spermatozoa from warm acclimated S. trutta males have longer flagella relative to their head size compared to their cold acclimated counterparts. This did not directly affect sperm swimming speed, although spermatozoa from warm acclimated males may have experienced a hydrodynamic advantage at warmer temperatures, as suggested by our calculations of drag based on head size and sperm swimming speed. The results presented here highlight the importance of increasing our knowledge of the effects of temperature on all aspects of salmonid reproduction in order to secure their continued abundance.

  • 6. Fitzpatrick, J. L.
    et al.
    Almbro, M.
    Gonzalez-Voyer, A.
    Hamada, S.
    Pennington, C.
    Scanlan, J.
    Kolm, Niclas
    Uppsala universitet, Zooekologi.
    Sexual selection uncouples the evolution of brain and body size in pinnipeds2012In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 25, no 7, p. 1321-1330Article in journal (Refereed)
    Abstract [en]

    The size of the vertebrate brain is shaped by a variety of selective forces. Although larger brains (correcting for body size) are thought to confer fitness advantages, energetic limitations of this costly organ may lead to trade-offs, for example as recently suggested between sexual traits and neural tissue. Here, we examine the patterns of selection on male and female brain size in pinnipeds, a group where the strength of sexual selection differs markedly among species and between the sexes. Relative brain size was negatively associated with the intensity of sexual selection in males but not females. However, analyses of the rates of body and brain size evolution showed that this apparent trade-off between sexual selection and brain mass is driven by selection for increasing body mass rather than by an actual reduction in male brain size. Our results suggest that sexual selection has important effects on the allometric relationships of neural development.

  • 7. Fitzpatrick, J. L.
    et al.
    Almbro, M.
    Gonzalez-Voyer, A.
    Kolm, Niclas
    Uppsala universitet, Zooekologi.
    Simmons, L. W.
    Male Contest Competition And The Coevolution Of Weaponry And Testes In Pinnipeds2012In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 66, no 11, p. 3595-3604Article in journal (Refereed)
    Abstract [en]

    Male reproductive success is influenced by competitive interactions during precopulatory and postcopulatory selective episodes. Consequently, males can gain reproductive advantages during precopulatory contest competition by investing in weaponry and during postcopulatory sperm competition by investing in ejaculates. However, recent theory predicts male expenditure on weaponry and ejaculates should be subject to a trade-off, and should vary under increasing risk and intensity of sperm competition. Here, we provide the first comparative analysis of the prediction that expenditure on weaponry should be negatively associated with expenditure on testes mass. Specifically, we assess how sexual selection influences the evolution of primary and secondary sexual traits among pinnipeds (seals, sea lions, and walruses). Using recently developed comparative methods, we demonstrate that sexual selection promotes rapid divergence in body mass, sexual size dimorphism (SSD), and genital morphology. We then show that genital length appears to be positively associated with the strength of postcopulatory sexual selection. However, subsequent analyses reveal that both genital length and testes mass are negatively associated with investment in precopulatory weaponry. Thus, our results are congruent with recent theoretical predictions of contest-based sperm competition models. We discuss the possible role of trade-offs and allometry in influencing patterns of reproductive trait evolution in pinnipeds.

  • 8. Fitzpatrick, J L
    et al.
    Desjardins, J K
    Milligan, N
    Stiver, K A
    Montgomerie, R
    Balshine, S
    Female-mediated causes and consequences of status change in a social fish.2008In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 275, no 1637Article in journal (Refereed)
    Abstract [en]

    In highly social species, dominant individuals often monopolize reproduction, resulting in reproductive investment that is status dependent. Yet, for subordinates, who typically invest less in reproduction, social status can change and opportunities to ascend to dominant social positions are presented suddenly, requiring abrupt changes in behaviour and physiology. In this study, we examined male reproductive anatomy, physiology and behaviour following experimental manipulations of social status in the cooperatively breeding cichlid fish, Neolamprologus pulcher. This unusual fish species lives in permanent social groups composed of a dominant breeding pair and 1-20 subordinates that form a linear social dominance hierarchy. By removing male breeders, we created 18 breeding vacancies and thus provided an opportunity for subordinate males to ascend in status. Dominant females play an important role in regulating status change, as males successfully ascended to breeder status only when they were slightly larger than the female breeder in their social group. Ascending males rapidly assumed behavioural dominance, demonstrated elevated gonadal investment and androgen concentrations compared with males remaining socially subordinate. Interestingly, to increase gonadal investment ascending males appeared to temporarily restrain somatic growth. These results highlight the complex interactions between social status, reproductive physiology and group dynamics, and underscore a convergent pattern of reproductive investment among highly social, cooperative species.

  • 9. Fitzpatrick, John L
    et al.
    Baer, Boris
    Polyandry reduces sperm length variation in social insects.2011In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 65, no 10Article in journal (Refereed)
    Abstract [en]

    Postcopulatory sexual selection, either in the form of sperm competition or cryptic female choice, is an important selective force that is thought to have generated the enormous variation in sperm morphology observed interspecifically. However, the evolutionary significance of intraspecific variation in sperm morphology, and the role that postcopulatory sexual selection plays in influencing this variation, remains poorly investigated in invertebrates. Here, we tested the hypothesis that postcopulatory sexual selection reduces variation in sperm morphology, both between and within males, in 27 species of eusocial ants and bees. These eusocial species offer an unusual opportunity to assess how selection acts on variance in sperm morphology, as haploid males produce clonal, haploid sperm that does not experience haploid-diploid conflict. We provide solid evidence that males of polyandrous ant and bee species indeed produce less-variable sperm, indicating that sperm competition selected for sperm of superior quality. Our results offer a mechanistic explanation for the evolution of high-quality sperm and provide comprehensive evidence that sperm morphology of social insects is influenced by sexual selection.

  • 10.
    Fitzpatrick, John L.
    et al.
    University of Manchester, UK; University of Western Australia, Australia.
    Evans, J. P.
    Postcopulatory inbreeding avoidance in guppies2014In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 27, no 12, p. 2585-2594Article in journal (Refereed)
    Abstract [en]

    In many species, the negative fitness effects of inbreeding have facilitated the evolution of a wide range of inbreeding avoidance mechanisms. Although avoidance mechanisms operating prior to mating are well documented, evidence for postcopulatory mechanisms of inbreeding avoidance remain scarce. Here, we examine the potential for paternity biases to favour unrelated males when their sperm compete for fertilizations though postcopulatory inbreeding avoidance mechanisms in the guppy, Poecilia reticulata. To test this possibility, we used a series of artificial inseminations to deliver an equal number of sperm from a related (either full sibling or half sibling) and unrelated male to a female while statistically controlling for differences in sperm quality between rival ejaculates. In this way, we were able to focus exclusively on postcopulatory mechanisms of inbreeding avoidance and account for differences in sperm competitiveness between rival males. Under these carefully controlled conditions, we report a significant bias in paternity towards unrelated males, although this effect was only apparent when the related male was a full sibling. We also show that sperm competition generally favours males with highly viable sperm and thus that some variance in sperm competitiveness can be attributed to difference in sperm quality. Our findings for postcopulatory inbreeding avoidance are consistent with prior work on guppies, revealing that sperm competition success declines linearly with the level of relatedness, but also that such effects are only apparent at relatedness levels of full siblings or higher. These findings reveal that postcopulatory processes alone can facilitate inbreeding avoidance.

  • 11.
    Fitzpatrick, John L.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Larson, Erica L.
    Finding Sperm in the English Countryside - The 14th Biology of Spermatozoa Meeting2018In: Molecular Reproduction and Development, ISSN 1040-452X, E-ISSN 1098-2795, Vol. 85, no 5, p. 371-373Article in journal (Refereed)
  • 12. Fitzpatrick, John L.
    et al.
    Montgomerie, Robert
    Desjardins, Julie K.
    Stiver, Kelly A.
    Kolm, Niclas
    Uppsala universitet, Institutionen för ekologi och evolution.
    Balshine, Sigal
    Female promiscuity promotes the evolution of faster sperm in cichlid fishes2009In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 106, no 4, p. 1128-1132Article in journal (Refereed)
    Abstract [en]

    Sperm competition, the contest among ejaculates from rival males to fertilize ova of a female, is a common and powerful evolutionary force influencing ejaculate traits. During competitive interactions between ejaculates, longer and faster spermatozoa are expected to have an edge; however, to date, there has been mixed support for this key prediction from sperm competition theory. Here, we use the spectacular radiation of cichlid fishes from Lake Tanganyika to examine sperm characteristics in 29 closely related species. We provide phylogenetically robust evidence that species experiencing greater levels of sperm competition have faster-swimming sperm. We also show that sperm competition selects for increases in the number, size, and longevity of spermatozoa in the ejaculate of a male, and, contrary to expectations from theory, we find no evidence of trade-offs among sperm traits in an interspecific analysis. Also, sperm swimming speed is positively correlated with sperm length among, but not within, species. These different responses to sperm competition at intra-and interspecific levels provide a simple, powerful explanation for equivocal results from previous studies. Using phylogenetic analyses, we also reconstructed the probable evolutionary route of trait evolution in this taxon, and show that, in response to increases in the magnitude of sperm competition, the evolution of sperm traits in this clade began with the evolution of faster (thus, more competitive) sperm.

  • 13. Fitzpatrick, Luisa J.
    et al.
    Gasparini, Clelia
    Fitzpatrick, John L.
    University of Manchester, UK.
    Evans, Jonathan P.
    Male-female relatedness and patterns of male reproductive investment in guppies2014In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 10, no 5Article in journal (Refereed)
    Abstract [en]

    Inbreeding can cause reductions in fitness, driving the evolution of pre- and postcopulatory inbreeding avoidance mechanisms. There is now considerable evidence for such processes in females, but few studies have focused on males, particularly in the context of postcopulatory inbreeding avoidance. Here, we address this topic by exposing male guppies (Poecilia reticulata) to either full-sibling or unrelated females and determining whether they adjust investment in courtship and ejaculates. Our results revealed that males reduce their courtship but concomitantly exhibit short-term increases in ejaculate quality when paired with siblings. In conjunction with prior work reporting cryptic female preferences for unrelated sperm, our present findings reveal possible sexually antagonistic counter-adaptations that may offset postcopulatory inbreeding avoidance by females.

  • 14. Fox, Graeme
    et al.
    Darolti, Iulia
    Hibbitt, Jean-Denis
    Preziosi, Richard F.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology. The University of Manchester, UK.
    Rowntree, Jennifer K.
    Bespoke markers for ex-situ conservation: application, analysis and challenges in the assessment of a population of endangered undulate rays2018In: Journal of Zoo and Aquarium Research, ISSN 2214-7594, Vol. 6, no 2, p. 50-56Article in journal (Refereed)
    Abstract [en]

    Genetic data are important and informative in the management of ex-situ populations. Where the risk of inbreeding is particularly great, it is critical that tools are employed that allow for the quantification of genetic variation and to identify potential breeding pairs. This study demonstrates the rapid application of laboratory and bioinformatics techniques to develop a novel microsatellite marker panel for use with a population of the endangered undulate ray (Raja undulata) and shows how a minimally invasive sampling method can be used with aquarium-dwelling individuals. The study assesses the population and investigates how informative a small microsatellite marker panel is to the conservation of a restricted ex-situ group. It was found that after a single captive generation of R. undulata there is no detectable evidence of reduced heterozygosity and no observable aquaria effects or differences between the generations. In conclusion, the study demonstrates that it is practical, quick and informative to develop a bespoke panel of markers to aid ex-situ conservation efforts of non-model species and make recommendations that these processes should constitute the minimum effort required in managing such a population.

  • 15.
    Gonzalez-Voyer, Alejandro
    et al.
    Uppsala universitet, Institutionen för ekologi och evolution.
    Fitzpatrick, John L.
    Kolm, Niclas
    Uppsala universitet, Institutionen för ekologi och evolution.
    Sexual selection determines parental care patterns in cichlid fishes2008In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 62, no 8, p. 2015-2026Article in journal (Refereed)
    Abstract [en]

    Despite a massive research effort, our understanding of why, in most vertebrates, males compete for mates and females care for offspring remains incomplete. Two alternative hypotheses have been proposed to explain the direction of causality between parental care and sexual selection. Traditionally, sexual selection has been explained as a consequence of relative parental investment, where the sex investing less will compete for the sex investing more. However, a more recent model suggests that parental care patterns result from sexual selection acting on one sex favoring mating competition and lower parental investment. Using species-level comparative analyses on Tanganyikan cichlid fishes we tested these alternative hypotheses employing a proxy of sexual selection based on mating system, sexual dichromatism, and dimorphism data. First, while controlling for female reproductive investment, we found that species with intense sexual selection were associated with female-only care whereas species with moderate sexual selection were associated with biparental care. Second, using contingency analyses, we found that, contrary to the traditional view, evolutionary changes in parental care type are dependent on the intensity of sexual selection. Hence, our results support the hypothesis that sexual selection determines parental care patterns in Tanganyikan cichlid fishes.

  • 16.
    Hansen Wheat, Christina
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Rogell, Björn
    Stockholm University, Faculty of Science, Department of Zoology.
    Temrin, Hans
    Stockholm University, Faculty of Science, Department of Zoology.
    Behavioural correlations of the domestication syndrome are decoupled in modern dog breeds2019In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 10, article id 2422Article in journal (Refereed)
    Abstract [en]

    Domestication is hypothesized to drive correlated responses in animal morphology, physiology and behaviour, a phenomenon known as the domestication syndrome. However, we currently lack quantitative confirmation that suites of behaviours are correlated during domestication. Here we evaluate the strength and direction of behavioural correlations among key prosocial (sociability, playfulness) and reactive (fearfulness, aggression) behaviours implicated in the domestication syndrome in 76,158 dogs representing 78 registered breeds. Consistent with the domestication syndrome hypothesis, behavioural correlations within prosocial and reactive categories demonstrated the expected direction-specificity across dogs. However, correlational strength varied between dog breeds representing early (ancient) and late (modern) stages of domestication, with ancient breeds exhibiting exaggerated correlations compared to modern breeds across prosocial and reactive behaviours. Our results suggest that suites of correlated behaviours have been temporally decoupled during dog domestication and that recent shifts in selection pressures in modern dog breeds affect the expression of domestication-related behaviours independently.

  • 17.
    Hansen Wheat, Christina
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Fitzpatrick, John
    Stockholm University, Faculty of Science, Department of Zoology.
    Tapper, Ingrid
    Temrin, Hans
    Stockholm University, Faculty of Science, Department of Zoology.
    Wolf (Canis lupus) hybrids highlight the importance of human-directed play behavior during domestication of dogs (Canis familiaris)Manuscript (preprint) (Other academic)
  • 18.
    Hansen Wheat, Christina
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Fitzpatrick, John
    Stockholm University, Faculty of Science, Department of Zoology.
    Temrin, Hans
    Stockholm University, Faculty of Science, Department of Zoology.
    Behavioural correlations of the domestication syndrome are decoupled in modern dog breedsManuscript (preprint) (Other academic)
  • 19. Kelley, Jennifer L.
    et al.
    Fitzpatrick, John L.
    The University of Western Australia, Australia.
    Merilaita, Sami
    Spots and stripes: ecology and colour pattern evolution in butterflyfishes2013In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 280, no 1757Article in journal (Refereed)
    Abstract [en]

    The incredible diversity of colour patterns in coral reef fishes has intrigued biologists for centuries. Yet, despite the many proposed explanations for this diversity in coloration, definitive tests of the role of ecological factors in shaping the evolution of particular colour pattern traits are absent. Patterns such as spots and eyespots (spots surrounded by concentric rings of contrasting colour) have often been assumed to function for predator defence by mimicking predators' enemies' eyes, deflecting attacks or intimidating predators, but the evolutionary processes underlying these functions have never been addressed. Striped body patterns have been suggested to serve for both social communication and predator defence, but the impact of ecological constraints remains unclear. We conducted the first comparative analysis of colour pattern diversity in butterflyfishes (Family: Chaetodontidae), fishes with conspicuous spots, eyespots and wide variation in coloration. Using a dated molecular phylogeny of 95 species (approx. 75% of the family), we tested whether spots and eyespots have evolved characteristics that are consistent with their proposed defensive function and whether the presence of spots and body stripes is linked with species' body length, dietary complexity, habitat diversity or social behaviour. Contrary to our expectations, spots and eyespots appeared relatively recently in butterflyfish evolution and are highly evolutionarily labile, suggesting that they are unlikely to have played an important part in the evolutionary history of the group. Striped body patterns showed correlated evolution with a number of ecological factors including habitat type, sociality and dietary complexity. Our findings question the prevailing view that eyespots are an evolutionary response to predation pressure, providing a valuable counter example to the role of these markings as revealed in other taxa.

  • 20. Lüpold, Stefan
    et al.
    Tomkins, Joseph L.
    Simmons, Leigh W.
    Fitzpatrick, John L.
    University of Western Australia, Australia; University of Manchester, UK.
    Female monopolization mediates the relationship between pre- and postcopulatory sexual traits2014In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 5, article id 3184Article in journal (Refereed)
    Abstract [en]

    Theory predicts a trade-off between investments in precopulatory (ornaments and armaments) and postcopulatory (testes and ejaculates) sexual traits due to the costs associated with their growth and maintenance within the finite energy resources available. Empirical studies, however, have revealed considerable inconsistency in the strength and direction of relationships among these sexual traits. Ambiguity may result from variance in the marginal benefits gained by increasing investments in either pre- or postcopulatory sexual traits. Here, in a broad comparative study, we test the prediction that the relationship between pre- and postcopulatory sexual traits differs among taxa relative to the importance of male-male contest competition within them. We find that covariance between pre- and postcopulatory sexual traits gradually shifts from strongly positive to strongly negative with increasing male-male contest competition. Thus, our findings reveal a potentially unifying explanation for the oftentimes inconsistent relationships in the strength and direction of covariance among sexual traits.

  • 21. Miller, Jessica S.
    et al.
    Bose, Aneesh P. H.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Balshine, Sigal
    Sperm maturation and male tactic-specific differences in ejaculates in the plainfin midshipman fish Porichthys notatus2019In: Journal of Fish Biology, ISSN 0022-1112, E-ISSN 1095-8649, Vol. 94, no 3, p. 434-445Article in journal (Refereed)
    Abstract [en]

    Using the plainfin midshipman fish Porichthys notatus, a species with alternative reproductive tactics (ARTs), we investigated how sperm maturation shapes sperm competitive abilities. We compared sperm performance and morphology before and after final sperm maturation by sampling sperm from the testes and stripped ejaculates of guarders and sneakers. In accordance with sperm competition risk theory, ejaculates from sneaker males had three times as much sperm as ejaculates from guarder males and sneaker males produced faster swimming sperm than guarder males, but this was only the case after final sperm maturation had occurred. Additionally, fully mature sperm found in ejaculates had larger heads and midpieces than sperm found in the testes. These results emphasize the important role played by non-sperm components of an ejaculate in mediating sperm performance and potentially also morphology.

  • 22.
    Rowley, Amy G.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Manchester, UK.
    Daly-Engel, Toby S.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Testes size increases with sperm competition risk and intensity in bony fish and sharks2019In: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 30, no 2, p. 364-371Article in journal (Refereed)
    Abstract [en]

    Female multiple mating provides the opportunity for sexual selection to continue after gamete release, generating strong selection on male reproductive traits. In particular, in species where female multiple mating is common, males are expected to invest more in testicular tissue to afford them a numerical advantage during sperm competition. However, although relative testes size (correcting for body size) is a commonly used proxy of the strength of sperm competition, there is surprisingly scant direct evidence linking male investment in testes with genetic estimates of multiple paternity across species. Here, we test the hypothesis that testes size is associated with genetic estimates of sperm competition risk (multiple paternity percentage) and intensity (number of sires per brood) in fishes, the most diverse and specious vertebrate group. We provide conclusive evidence that relative testes size is larger in species experiencing a higher risk and intensity of sperm competition, a finding that remains consistent among sharks and bony fishes (including in separate analyses focused only on cichlids). These findings shed new light on evolutionary processes governing sperm competition in a basal vertebrate lineage and validate the now-widespread use of relative testes mass as a proxy for sperm competition risk and intensity in fishes.

  • 23.
    Rowley, Amy
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University of Manchester, UK.
    Locatello, Lisa
    Kahrl, Ariel
    Stockholm University, Faculty of Science, Department of Zoology.
    Rego, Mariana
    Boussard, Annika
    Stockholm University, Faculty of Science, Department of Zoology.
    Garza-Gisholt, Eduardo
    Kempster, Ryan M.
    Collin, Shaun P.
    Giacomello, Eva
    Follesa, Maria C.
    Porcu, Cristina
    Evans, Jonathan P.
    Hazin, Fabio
    Garcia-Gonzalez, Francisco
    Daly-Engel, Toby
    Mazzoldi, Carlotta
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Sexual selection and the evolution of sperm morphology in sharks2019In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101Article in journal (Refereed)
    Abstract [en]

    Post-copulatory sexual selection, and sperm competition in particular, is a powerful selective force shaping the evolution of sperm morphology. Although mounting evidence suggests that post-copulatory sexual selection influences the evolution of sperm morphology among species, recent evidence also suggests that sperm competition influences variation in sperm morphology at the intraspecific level. However, contradictory empirical results and limited taxonomic scope have led to difficulty in assessing the generality of sperm morphological responses to variation in the strength of sperm competition. Here, we use phylogenetically controlled analyses to explore the effects of sperm competition on sperm morphology and variance in sharks, a basal vertebrate group characterized by wide variation in rates of multiple mating by females, and consequently sperm competition risk. Our analyses reveal that shark species experiencing greater levels of sperm competition produce sperm with longer flagella and that sperm flagellum length is less variable in species under higher sperm competition risk. In contrast, neither the length of the sperm head and midpiece nor variation in sperm head and midpiece length was associated with sperm competition risk. Our findings demonstrate that selection influences both the inter- and intraspecific variation in sperm morphology and suggest that the flagellum is an important target of sexual selection in sharks. These findings provide important insight into patterns of selection on the ejaculate in a basal vertebrate lineage.

  • 24. Simmons, Leigh W.
    et al.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Female genitalia can evolve more rapidly and divergently than male genitalia2019In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 10, article id 1312Article in journal (Refereed)
    Abstract [en]

    Male genitalia exhibit patterns of divergent evolution driven by sexual selection. In contrast, for many taxonomic groups, female genitalia are relatively uniform and their patterns of evolution remain largely unexplored. Here we quantify variation in the shape of female genitalia across onthophagine dung beetles, and use new comparative methods to contrast their rates of divergence with those of male genitalia. As expected, male genital shape has diverged more rapidly than a naturally selected trait, the foretibia. Remarkably, female genital shape has diverged nearly three times as fast as male genital shape. Our results dispel the notion that female genitalia do not show the same patterns of divergent evolution as male genitalia, and suggest that female genitalia are under sexual selection through their role in female choice.

  • 25. Simmons, Leigh W.
    et al.
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Sperm competition and the coevolution of pre- and postcopulatory traits: Weapons evolve faster than testes among onthophagine dung beetles2016In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 5, p. 998-1008Article in journal (Refereed)
    Abstract [en]

    Reproductive competition generates episodes of both pre- and postcopulatory sexual selection. Theoretical models of sperm competition predict that as the fitness gains from expenditure on the weapons of male combat increase, males should increase their expenditure on weapons and decrease their expenditure on traits that contribute to competitive fertilization success. Although traits subject to sexual selection are known to have accelerated evolutionary rates of phenotypic divergence, it is not known whether the competing demands of investment into pre- and postcopulatory traits affect their relative rates of evolutionary divergence. We use a comparative approach to estimate the rates of divergence in pre-and postcopulatory traits among onthophagine dung beetles. Weapons evolved faster than body size while testes mass and sperm length evolved more slowly than body size, suggesting that precopulatory competition is the stronger episode of sexual selection acting on these beetles. Although horns evolved faster than testes, evolutionary increases in horn length were not associated with evolutionary reductions in testes mass. Our data for onthophagines support the notion that in taxa where males are unable to monopolize paternity, expenditure on both weapons and testes should both be favored.

  • 26. Simmons, Leigh W.
    et al.
    Lüpold, Stefan
    Fitzpatrick, John L.
    Stockholm University, Faculty of Science, Department of Zoology.
    Evolutionary Trace-Off between Seconcary Sexual Traits and Ejaculates2017In: Trends in Ecology & Evolution, ISSN 0169-5347, E-ISSN 1872-8383, Vol. 32, no 12, p. 964-976Article, review/survey (Refereed)
    Abstract [en]

    Recent theoretical models predict that the evolutionary diversification of the weapons and ornaments of pre-mating sexual selection should be influenced by trade-offs with male expenditure on ejaculates. However, the patterns of association between secondary sexual traits and ejaculate expenditure are frequently inconsistent in their support of this prediction. We show why consideration of additional life-history, ecological, and mating-system variables is crucial for the interpretation of associations between secondary sexual traits and ejaculate production. Incorporation of these 'missing variables' provides evidence that interactions between pre- and post-mating sexual selection can underlie broad patterns of diversification in male weapons and ornaments. We call for more experimental and genetic approaches to uncover trade-offs, as well as for studies that consider the costs of mate-searching.

  • 27.
    Wheat, Christina Hansen
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Fitzpatrick, John
    Stockholm University, Faculty of Science, Department of Zoology.
    Tapper, Ingrid
    Temrin, Hans
    Stockholm University, Faculty of Science, Department of Zoology.
    Wolf (Canis lupus) Hybrids Highlight the Importance of Human-Directed Play Behavior During Domestication of Dogs (Canis familiaris)2018In: Journal of comparative psychology (1983), ISSN 0735-7036, E-ISSN 1939-2087, Vol. 132, no 4, p. 373-381Article in journal (Refereed)
    Abstract [en]

    The domestication of animals and plants offers an exceptional opportunity to study evolutionary adaptations. In particular, domesticated animals display several behavioral alterations, including increased sociability and decreased fearfulness and aggression, when compared with their wild ancestors. However, studies quantifying simultaneous changes in multiple behaviors during domestication are lacking. Moreover, the role of human-directed play behavior has been largely neglected when studying the domestication process. Here we address these issues by examining behavioral changes during the domestication of the dog (Canis familiaris) from the gray wolf (Canis lupus) using a standardized behavioral test applied to wolf hybrids and several dog breeds. Contrary to expectations, our study provides little support for collective behavioral alterations. Specifically, although we found that wolf hybrids were less playful and overall more fearful than dogs, we did not detect any differences in sociability or aggression between wolf hybrids and dog breeds. Instead, our results suggest that behavioral alterations during domestication do not necessarily occur in concert and point to an important, but previously overlooked, role of selection on play behavior directed at humans during the domestication of dogs.

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