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  • 1.
    de Boer, Raïssa A.
    et al.
    University of Antwerp, Belgium.
    Eens, Marcel
    Fransen, Erik
    Müller, Wendt
    Hatching asynchrony aggravates inbreeding depression in a songbird (Serinus canaria): An inbreeding–environment interaction2015In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 69, no 4, p. 1063-1068Article in journal (Refereed)
    Abstract [en]

    Understanding how the intensity of inbreeding depression is influenced by stressful environmental conditions is an important area of enquiry in various fields of biology. In birds, environmental stress during early development is often related to hatching asynchrony; differences in age, and thus size, impose a gradient in conditions ranging from benign (first hatched chick) to harsh (last hatched chick). Here, we compared the effect of hatching order on growth rate in inbred (parents are full siblings) and outbred (parents are unrelated) canary chicks (Serinus canaria). We found that inbreeding depression was more severe under more stressful conditions, being most evident in later hatched chicks. Thus, consideration of inbreeding‐environment interactions is of vital importance for our understanding of the biological significance of inbreeding depression and hatching asynchrony. The latter is particularly relevant given that hatching asynchrony is a widespread phenomenon, occurring in many bird species. The exact causes of the observed inbreeding‐environment interaction are as yet unknown, but may be related to a decrease in maternal investment in egg contents with laying position (i.e. prehatching environment), or to performance of the chicks during sibling competition and/or their resilience to food shortage (i.e. posthatching environment).

  • 2.
    de Boer, Raïssa A.
    et al.
    University of Antwerp, Belgium.
    Eens, Marcel
    Müller, Wendt
    A loss of heterozygosity, a loss in competition? The effects of inbreeding, pre- and postnatal conditions on nestling development.2016In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 6, no 21, p. 7921-7930Article in journal (Refereed)
    Abstract [en]

    The early developmental trajectory is affected by genetic and environmental factors that co-depend and interact often in a complex way. In order to distinguish their respective roles, we used canaries (Serinus canaria) of different genetic backgrounds (inbred and outbred birds). An artificial size hierarchy was created to provoke within-nest competition, manipulating postnatal conditions. To this end, inbred birds were weight-matched with outbred birds into duos, and each nest contained one duo of size-advantaged, and one duo of size-disadvantaged inbred and outbred nestlings. Prenatal (maternal) effects were taken into account also, enabling us to study the separate as well as the interactive effects of inbreeding, pre- and postnatal conditions on nestling development. We find that postnatal conditions were the most important determinant of early growth, with size-advantaged nestlings growing faster and obtaining larger size/body mass at fledging in comparison with size-disadvantaged nestlings. Prenatal conditions were important too, with birds that hatched from eggs that were laid late in the laying order obtaining a larger size at fledging than those hatched from early laid eggs. Inbreeding inhibited growth, but surprisingly this did not depend on (dis)advantageous pre- or postnatal conditions. Our findings imply that inbred individuals lose when they are in direct competition with same-sized outbred individuals regardless of the rearing conditions, and we thus propose that reduced competitiveness is one of the driving forces of inbreeding depression.

  • 3.
    de Boer, Raïssa A.
    et al.
    University of Antwerp, Belgium.
    Eens, Marcel
    Müller, Wendt
    An experimental study: Does inbreeding increase the motivation to mate?2018In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 13, no 6, article id e0199182Article in journal (Refereed)
    Abstract [en]

    Inbreeding is a central topic in evolutionary biology and ecology and is of major concern for the conservation of endangered species. Yet, it remains challenging to comprehend the fitness consequences of inbreeding, because studies typically focus only on short-term effects on inbreeding in the offspring (e.g. survival until independence). However, there is no a priori reason to assume that inbreeding has no more effects in adulthood. Specifically, inbred males should have lower reproductive success than outbred males among other things because of inbreeding depression in attractiveness to females and a reduced lifespan. Such differences in future reproductive value should affect male mating behaviour, such that an inbred male of a given age should be more motivated to seize a current mating opportunity than an outbred male of the same age. We used an inventive experimental set-up that enabled us to assess male behaviour in relation to an apparent mating opportunity while excluding potential confounding effects of female preference. Age-, weight-, and size-matched inbred and outbred male canaries (Serinus canaria) were presented with a female that only one male at a time could access visually via a ‘peephole’ and thus when both males were equally interested in seizing the apparent mating opportunity this would result in contest. We find that inbred males spent more than twice as much time ‘peeping’ at the female than outbred males, suggesting that inbreeding indeed causes different behavioural responses to an apparent mating opportunity. Our study is among the first to highlight that inbreeding affects male mating behaviour, and therewith potentially male-male competition, which should be taken into account in order to understand the full range of inbreeding effects on fitness.

  • 4.
    de Boer, Raïssa A.
    et al.
    University of Antwerp, Belgium.
    Eens, Marcel
    Müller, Wendt
    'Out of tune': consequences of inbreeding on bird song2016In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 283, no 1835, article id 20161142Article in journal (Refereed)
    Abstract [en]

    The expression of bird song is expected to signal male quality to females. 'Quality' is determined by genetic and environmental factors, but, surprisingly, there is very limited evidence if and how genetic aspects of male quality are reflected in song. Here, we manipulated the genetic make-up of canaries (Serinus canaria) via inbreeding, and studied its effects upon song output, complexity, phonetics and, for the first time, song learning. To this end, we created weight-matched inbred and outbred pairs of male fledglings, which were subsequently exposed to the same tutor male during song learning. Inbreeding strongly affected syllable phonetics, but there were little or no effects on other song features. Nonetheless, females discriminated among inbred and outbred males, as they produced heavier clutches when mated with an outbred male. Our study highlights the importance of song phonetics, which has hitherto often been overlooked.

  • 5.
    de Boer, Raïssa A.
    et al.
    University of Antwerp, Belgium.
    Eens, Marcel
    Müller, Wendt
    Sex-specific effects of inbreeding on reproductive senescence2018In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 285, no 1879, article id 20180231Article in journal (Refereed)
    Abstract [en]

    Inbreeding depression plays a significant role in evolutionary biology and ecology. However, we lack a clear understanding of the fitness consequences of inbreeding depression. Studies often focus on short-term effects of inbreeding in juvenile offspring, whereas inbreeding depression in adult traits and the interplay between inbreeding depression and age are rarely addressed. Inbreeding depression may increase with age and accelerate the decline in reproductive output in ageing individuals (reproductive senescence), which could be subject to sex-specific dynamics. We test this hypothesis with a longitudinal experimental study in a short-lived songbird. Adult inbred and outbred male and female canaries were paired in a 2 × 2 factorial design, and survival and annual reproductive performance were studied for 3 years. We found inbreeding depression in female egg-laying ability, male fertilization success and survival of both sexes. Annual reproductive success of both males and females declined when paired with an inbred partner independent of their own inbreeding status. This shows that inbreeding can have fitness costs in outbred individuals when they mate with an inbred individual. Further, inbred females showed faster reproductive senescence than outbred females, confirming that inbreeding depression and age can interact to affect fitness. By contrast, there was no evidence for an interaction between inbreeding depression and reproductive senescence in male fertilization success. Our findings highlight the importance of considering sex-specific effects and age to determine the full range of fitness consequences of inbreeding and demonstrate that inbreeding depression can accelerate reproductive senescence.

  • 6.
    de Boer, Raïssa A.
    et al.
    Biomedical Primate Research Center, The Netherlands; Utrecht University, The Netherlands.
    Overduin-de Vries, Anne M.
    Louwerse, Annet L.
    Sterck, Elisabeth H. M.
    The behavioral context of visual displays in common marmosets (Callithrix jacchus)2013In: American Journal of Primatology, ISSN 0275-2565, E-ISSN 1098-2345, Vol. 75, no 11, p. 1084-1095Article in journal (Refereed)
    Abstract [en]

    Communication is important in social species, and may occur with the use of visual, olfactory or auditory signals. However, visual communication may be hampered in species that are arboreal have elaborate facial coloring and live in small groups. The common marmoset fits these criteria and may have limited visual communication. Nonetheless, some (contradictive) propositions concerning visual displays in the common marmoset have been made, yet quantitative data are lacking. The aim of this study was to assign a behavioral context to different visual displays using pre–post‐event‐analyses. Focal observations were conducted on 16 captive adult and sub‐adult marmosets in three different family groups. Based on behavioral elements with an unambiguous meaning, four different behavioral contexts were distinguished: aggression, fear, affiliation, and play behavior. Visual displays concerned behavior that included facial expressions, body postures, and pilo‐erection of the fur. Visual displays related to aggression, fear, and play/affiliation were consistent with the literature. We propose that the visual display “pilo‐erection tip of tail” is related to fear. Individuals receiving these fear signals showed a higher rate of affiliative behavior. This study indicates that several visual displays may provide cues or signals of particular social contexts. Since the three displays of fear elicited an affiliative response, they may communicate a request of anxiety reduction or signal an external referent. Concluding, common marmosets, despite being arboreal and living in small groups, use several visual displays to communicate with conspecifics and their facial coloration may not hamper, but actually promote the visibility of visual displays.

  • 7.
    de Boer, Raïssa Anna
    et al.
    University of Antwerp, Belgium.
    Costantini, David
    Casasole, Giulia
    AbdElgawad, Hamada
    Asard, Han
    Eens, Marcel
    Müller, Wendt
    Sex-specific effects of inbreeding and early life conditions on the adult oxidative balance2018In: Current Zoology, ISSN 1674-5507, Vol. 64, no 5, p. 631-639Article in journal (Refereed)
    Abstract [en]

    Inbreeding negatively affects various life-history traits, with inbred individuals typically having lower fitness than outbred individuals (= inbreeding depression). Inbreeding depression is often emphasized under environmental stress, but the underlying mechanisms and potential long-lasting consequences of such inbreeding-environment interactions remain poorly understood. Here, we hypothesize that inbreeding-environment interactions that occur early in life have long-term physiological effects, in particular on the adult oxidative balance. We applied a unique experimental design to manipulate early life conditions of inbred and outbred songbirds (Serinus canaria) that allowed us to separate prenatal and postnatal components of early life conditions and their respective importance in inbreeding-environment interactions. We measured a wide variety of markers of oxidative status in adulthood, resulting in a comprehensive account for oxidative balance. Using a Bayesian approach with Markov chain Monte Carlo, we found clear sex-specific effects and we also found only in females small yet significant long-term effects of inbreeding-environment interactions on adult oxidative balance. Postnatal components of early life conditions were most persuasively reflected on adult oxidative balance, with inbred females that experienced disadvantageous postnatal conditions upregulating enzymatic antioxidants in adulthood. Our study provides some evidence that adult oxidative balance can reflect inbreeding-environment interactions early in life, but given the rather small effects that were limited to females, we conclude that oxidative stress might have a limited role as mechanism underlying inbreeding-environment interactions.

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