Mate preference of female blue tits varies with experimental photoperiod.

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Mate Preference of Female Blue Tits Varies with Experimental Photoperiod Laura B. Reparaz1,2, Kees van Oers1, Marc Naguib2, Claire Doutrelant3, Marcel E. Visser1, Samuel P. Caro1,3* 1 Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands, 2 Behavioural Ecology Group, Department of Animal Sciences, Wageningen University (WUR), The Netherlands, 3 Department of Evolutionary Ecology, CEFE-CNRS, Montpellier, France Abstract Organisms use environmental cues to time their life-cycles and among these cues, photoperiod is the main trigger of reproductive behaviours such as territory defence or song activity. Whether photoperiod is also important for another behaviour closely associated with reproduction, mate choice, is unknown. In many bird species, mate choice occurs at two different times during the annual cycle that strongly differ in daylength: in late winter when photoperiod is short and social mates are chosen, and again around egg-laying when photoperiod is longer and extra-pair mates are chosen. This duality makes the role that photoperiod plays on mate choice behaviours intriguing. We investigated the effect of photoperiod on mate choice using three experimental photoperiodic treatments (9 L:15 D, 14 L:10 D, 18 L:6 D), using blue tits (Cyanistes caeruleus) as a biological model. We show that female choice was stronger under long photoperiods. In addition, female blue tits spent significantly more time near males with long tarsi and long wings. This latter preference was only expressed under long photoperiods, suggesting that some indices of male quality only become significant to females when they are strongly photostimulated, and therefore that females could select their social and extra-pair mates based on different phenotypic traits. These results shed light on the roles that photoperiod may play in stimulating pair-bonding and in refining female selectivity for male traits. Citation: Reparaz LB, van Oers K, Naguib M, Doutrelant C, Visser ME, et al. (2014) Mate Preference of Female Blue Tits Varies with Experimental Photoperiod. PLoS ONE 9(3): e92527. doi:10.1371/journal.pone.0092527 Editor: Paul A. Bartell, Pennsylvania State University, United States of America Received October 10, 2013; Accepted February 24, 2014; Published March 26, 2014 Copyright: ß 2014 Reparaz et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the Netherlands Organisation for Scientific Research (NWO) [VICI-grant to M.E.V., VENI-grant to S.P.C.], and by WallonieBruxelles International (WBI) [World-grant to S.P.C.]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: samuel.caro@cefe.cnrs.fr direct and indirect benefits, such as parental care, genetic quality for the offspring or access to a high quality territory, can be derived from selecting an appropriate partner [8]. As mate choice is a crucial prerequisite for breeding, one might predict that it is influenced by environmental factors and mechanisms similar to those that determine reproduction, including photoperiod [9]. Long photoperiods could enhance an animal’s selectivity for particular traits that are only relevant in a sexual context, and not outside the breeding cycle [10,11]. In meadow voles (Microtus pennsylvanicus) for instance, exposing females to long days is sufficient to reverse their winter-typical preference for female odours to a summer-typical preference for male odours [12]. In birds, female canaries (Serinus canaria) are responsive to male song only after being exposed to long photoperiods, an effect that intesifies when they reach fertility [13]. In many bird species, including those considered monogamous, individuals mate with more than one partner within a single breeding season. In the blue tit (Cyanistes caeruleus), the subject of the current study, up to 68% of females engage in copulations with males that are different from their social partner [14,15]. The choice to engage in extra-pair copulations is made around egglaying [16–19], while the social mate is typically chosen much earlier, in late winter [20,21]. This illustrates that mate choosing behaviours are not only important before reproduction starts, but Introduction In temperate zones, most animal species start breeding remarkably regularly each year. The short time-window dedicated to reproduction generally occurs in spring, when temperatures are mild and large amounts of nutrient- and protein-rich food necessary for raising offspring become available. To time and organize the complex temporal pattern of reproductive behaviours, animals use environmental cues that predict, well in advance, the onset of suitable conditions for breeding [1,2]. Among these cues, the most reliable predictive signal is the annual change in photoperiod: every year, favourable spring conditions for breeding coincide with a progressive increase in day length. Exposure to increasingly longer photoperiods triggers a cascade of neuroendocrine reactions that prepare animals for breeding: e.g., genes are activated in the brain, reproductive hormones increase in concentration in the blood, and gonads mature and start producing gametes [3–6]. These physiological changes in turn stimulate the expression of a complex and well-organized suite of reproductive behaviours such as territory defence, courting, nest preparation and communication displays, like songs in songbirds [1]. Another behaviour that is closely associated with reproduction is mate choice. Mate choice is a key life-history decision that impacts an individual’s current reproductive success and fitness [7]. Both PLOS ONE | www.plosone.org 1 March 2014 | Volume 9 | Issue 3 | e92527 Photoperiod Influences Mate Choice photoperiods. Whole broods of chicks (N = 7 broods at Muro, 10 broods at Pirio) were collected from their nests when they were 10day-olds, and were transferred to the laboratory for standardized hand rearing [33,34]. Briefly, birds were transported to the Netherlands Institute of Ecology (NIOO-KNAW) by car in natural nests in three wooden boxes (30614 cm and 10 cm high divided into three compartments, each containing one nest). These three boxes were placed into a larger wooden box that helped maintain temperature and humidity at optimal levels for chicks of this age (around 25uC and 50% humidity). If necessary, electric warming pads (ThermoLux, Murrhardt, Germany) were placed under the large box to provide extra heating. During the travel, and later on at the institute, chicks were fed every half-hour, for 14 hours per day (7:00 am–9:00 pm), with a diet consisting of a mixture of curd cheese, ground beef heart, baby cereal, multivitamin solution and calcium carbonate, supplemented with wax moth larvae and bee larvae, until independence. After reaching independence (about 35 days after hatching), the birds were transferred to an individual home cage of 0.960.4 m60.5 m high with solid bottom, top, side and rear walls, a wire-mesh front and three perches. As part of a previous experiment, half of the birds had been gradually experiencing a lengthening photoperiod (14 L:10 D), by increments of 38 minutes per week, while the other half of the birds had been moved directly to a constant long photoperiod (14 L:10 D). At the beginning of the present experiment, therefore, birds were photostimulated with a 14 L:10 D light schedule. These pre-treatments did not impact any of the response variables measured in the present experiment (all P-values .0.05), and will not be further considered. For the present experiment, all birds were housed individually in cages (identical to those described above) in single-sex rooms. Temperature in the rooms was kept between 15 and 17uC. Birds had visual and auditory contact with each other. Diet consisted of a mixture of egg, cow heart, dry bird food, vitamins, and minerals, supplemented with dry food containing insects, peanuts, and vitamins. Birds also had access to mealworms, grit, and sunflower seeds. Food and water were provided ad libitum. At the end of the experiment, birds that were not used for other research purposes were released into their population of origin in Corsica. This reintroduction took place in mid-March 2012, a time when temperatures are mild in Corsica and food is abundant. During transportation, adult birds were housed in wooden boxes (100630 cm615 cm high, divided into 6 compartments, one bird per compartment) where they received their normal diet (see above). also during the breeding season, for selecting individuals with whom to potentially engage in extra-pair copulations. Given that these two time periods strongly differ in their day length, the role that photoperiod plays on mate choice behaviours in these species is intriguing. The potential photoperiodic modulation of female selectivity for male traits could lead to differences in the criteria used by females for choosing social mates in late winter, and extrapair mates during longer days in the breeding season. In great tits (Parus major), for instance, females select extra-pair mates during the breeding season based on personality traits [22], while there is no clear evidence that they do so for their social mates that are chosen under a shorter photoperiod [23,24]. Here, we examine the relationship between photoperiod and mate choice behaviours in captive blue tits. The birds we study originate from the long-term Corsican study sites of Muro and Pirio, which strongly differ in their habitat characteristics and selection pressures [25]. Birds from these two sites fundamentally vary in a number of characteristics, including laying dates that occur one month apart [26–28]. Experiments in captivity have suggested that these population differences in reproductive traits resulted from a different response to photoperiod [29,30]: early breeding birds from Muro have a lower response threshold to photoperiod (i.e., respond to shorter photoperiods) than latebreeding birds from Pirio. By specifically investigating the effect of photoperiod on mate choice between Muro and Pirio birds, population-specific patterns can be identified that shed light on photoperiodic effects on mate choice in general. In particular, if Muro birds have a lower response threshold to photoperiod, we expect mate choice-related behaviours to be enhanced by comparatively shorter photoperiods in Muro birds than in Pirio birds. The primary aim of this study therefore is to identify the impact of photoperiod and origin population on the general interest of females in males and on their strength of preference for a particular male. Because females attend to various male traits, and because a female’s choice could be influenced by her own traits [31], we quantified female mate choice in relation to both male and female biometric traits (tarsus and wing lengths) that reflect their intrinsic qualities [16]. Moreover, we explore how personality [22,32] influences both male attractiveness and female decision rules, and whether these are dependent on the photoperiod to which birds are exposed. If birds choose different kinds of mates (social vs. extra-pair) based on different indices of quality, we predict that some of these morphological and behavioural traits will only affect mate choice behaviours under some photoperiods and not others. Novel Environment Test Methods Directly before the start of the experiment, birds were tested using the novel environment test modified from Verbeek et al. [35], an established operational measure of avian personality. All individuals were tested individually in a room (4.062.462.5 m) with five artificial wooden ‘trees’. Test-subjects were housed adjacent to the test room, in cages equipped with sliding doors leading to the test room. Test-subjects were placed in the cages 30–120 minutes before testing. The test-subject was introduced into the room without being handled, by darkening the subject’s cage with a draped towel, and opening the sliding door that connected the cage to the test room. After the sliding door was opened, the observer turned on the light in the test room. Once the test-subject entered the room, its movements were observed for two minutes, after which the trial ended, and the subject was returned to its home cage. The total number of movements between the five trees was counted, as well as hops up, down, and along branches of each tree, and based on these measures, birds Ethics Statement The experiments run in this study were approved by the Animal Experimentation Committee of the Royal Dutch Academy of Sciences (DEC-KNAW; permit number CTE.09–04 and NIOO11.09). The work performed in the field was approved by the prefectural office of Corsica and the Regional Direction of Environment (DIREN) committee (permit numbers 2009–0379 and 3467). Subjects We used sixty-seven second calendar year (hatched in 2010) captive Corsican blue tits (34 females, 33 males) for the experiment, all originating from Muro or Pirio populations in Corsica. These populations are located at similar latitudes, and therefore experience similar absolute, and annual variation in, PLOS ONE | www.plosone.org 2 March 2014 | Volume 9 | Issue 3 | e92527 Photoperiod Influences Mate Choice sexes are always simultaneously exposed to identical photoperiods. Testing female choice for males that are in a completely different physiological state than that of the female would thus have been highly artificial. We quantified male activity and behaviours while in the presence of a female to assess the effect of photoperiod on male behaviours. No effects were found (see table S2), and therefore the effect of photoperiod on female behaviours is not driven through its effect on male behaviours. While each female was only tested once, due to a limited number of available males, each male pair was used in two to four mate choice trials. The different photoperiods followed each other during the course of the experiment. This means that the effect of daylength was confounded with the effect of date. Females’ choice might therefore have been affected by this date effect, especially if it was their endogenous clock, rather than photoperiod, that was triggering the observed behavioural changes. Note however, that the photoperiods experienced by the birds mimicked the natural order of photoperiodic changes for a bird in spring (i.e., long - very long - short photoperiod). Thus, like in the real world, the birds were exposed to different daylengths at different times of the year, and therefore any influence of the endogenous clock that would occur here, would also occur in the wild. In addition, we tested a different group of females in each of the photoperiodic treatments (i.e., individual females were tested only once), meaning that there is no order effect due to females tested multiple times in the same succession of treatments. Finally, birds remained at least two weeks under each photoperiod before behavioural testing occurred, which is sufficient to ellicit robust and relatively stable changes in physiological states, with a minimal impact of past photoperiods (see above). were given an exploratory score on a continuous scale with higher scores indicating faster exploration, and lower scores indicating slower exploration. Exploration scores of birds in our experiment varied from 10 (very slow) to 92 (very fast). Photoperiodic treatments and pairing Blue tits from both Muro and Pirio were exposed to three different photoperiodic treatments (9, 14, and 18 hours of light per day - 9 L:15 D, 14 L:10 D, and 18 L:6 D). These photoperiods respectively correspond to the minimum photoperiod encountered in winter in Corsica, the photoperiod at which Corsican blue tits breed, and an artificially long photoperiod often used in captive experiments investigating the effect of day length on birds’ behaviour and physiology [36,37,38]. Photoperiodic treatments were applied sequentially to all birds, as space limitations prevented a set-up in which the three different treatments were run simultaneously to different groups of birds housed in different rooms. As a consequence, the effect of photoperiod was confounded with date (but see below). At the start of the experiment, birds were exposed to a 14 L:10 D schedule, for two weeks (see above). During the last two days of the 14 L:10 D schedule, a group of 11 females (consisting of both Muro and Pirio birds) was mate choice tested. After this first group of females had been tested, the photoperiod of the single-sex rooms was switched to 18 L:6 D, and at the end of two weeks, another group of 11 (previously-untested) females was tested over two days. The photoperiod of the single-sex rooms was then switched to the final treatment, 9 L:15 D. At the end of two weeks at 9 L:15 D, a final group of 12 (previously-untested) females was mate choice tested. Thus, a total of 34 females were mate choice tested in this experiment, meaning that the females that were tested under one given treatment were never re-used later. See table S1 for a summary of female mate choice testing by origin population and photoperiodic treatment. Two weeks of treatment is sufficient to elicit stable and robust neuroendocrine responses and their associated behaviours in birds. In Japanese quails (Coturnix coturnix japonica), for example, brain activity and circulating luteinizing hormone (LH) concentrations start increasing within hours after the transfer to long photoperiods and reach their maximum within a few days [39]. In starlings (Sturnus vulgaris), maximal enfocar la importancia de la producción mediática de los niños en su descubrimiento del mundo, sobre todo utilizando el periódico escolar y la imprenta. Asimismo las asociaciones de profesores trabajaron en esta línea e incluso la enseñanza católica se comprometió desde los años sesenta realizando trabajos originales en el marco de la corriente del Lenguaje Total. Páginas 43-48 45 Comunicar, 28, 2007 En el ámbito de los medios, también desde el principio del siglo XX hay ciertas corrientes de conexión. Pero es a lo largo de los años sesenta cuando se constituyeron asociaciones de periodistas apasionados por sus funciones de mediadores, que fomentaron la importancia ciudadana de los medios como algo cercano a los jóvenes, a los profesores y a las familias. Así se crearon la APIJ (Asociación de Prensa Información para la Juventud), la ARPEJ (Asociación Regional de Prensa y Enseñanza para la Juventud), el CIPE (Comité Interprofesional para la Prensa en la Escuela) o la APE (Asociación de Prensa y Enseñanza), todas ellas para la prensa escrita Estas asociaciones fueron precedidas por movimientos surgidos en mayo de 1968, como el CREPAC que, utilizando películas realizadas por periodistas conocidos, aclaraba temas que habían sido manipulados por una televisión demasiado próxima al poder político y realizaba encuentros con grupos de telespectadores. cipio del siglo XX, y nos han legado textos fundadores muy preciados, importantes trabajos de campo y muchos logros educativos y pedagógicos. La educación en medios ha tenido carácter de oficialidad de múltiples maneras, aunque nunca como una enseñanza global. Así la campaña «Operación Joven Telespectador Activo» (JTA), lanzada al final de los años setenta y financiada de manera interministerial para hacer reflexionar sobre las prácticas televisuales de los jóvenes, la creación del CLEMI (Centro de Educación y Medios de Comunicación) en el seno del Ministerio de Educación Nacional en 1983, la creación de la optativa «Cine-audiovisual» en los bachilleratos de humanidades de los institutos en 1984 (primer bachillerato en 1989) y múltiples referencias a la educación de la imagen, de la prensa, de Internet. La forma más visible y rápida de evaluar el lugar de la educación en medios es valorar el lugar que se le ha reservado en los libros de texto del sistema educa- 2. Construir la educación en los medios sin nombrarla El lugar que ocupa la edu- La denominación «educación en medios», que debería cación en los medios es muy ambiguo, aunque las cosas están cambiando recientemente. entenderse como un concepto integrador que reagrupase todos los medios presentes y futuros, es a menudo percibida En principio, en Francia, co- por los «tradicionalistas de la cultura» como una tendencia mo en muchos otros países, la educación en los medios no es hacia la masificación y la pérdida de la calidad. una disciplina escolar a tiempo completo, sino que se ha ido conformado progresivamente a través de experiencias y reflexiones teóricas que han tivo en Francia. Una inmersión sistemática nos permi- permitido implantar interesantes actividades de carác- te constatar que los textos oficiales acogen numerosos ter puntual. Se ha ganado poco a poco el reconoci- ejemplos, citas, sin delimitarla con precisión. miento de la institución educativa y la comunidad es- colar. Podemos decir que ha conquistado un «lugar», 3. ¿Por qué la escuela ha necesitado casi un siglo en el ámbito de la enseñanza transversal entre las dis- para oficilializar lo que cotidianamente se hacía en ciplinas existentes. ella? Sin embargo, la escuela no está sola en esta aspi- Primero, porque las prácticas de educación en me- ración, porque el trabajo en medios es valorado igual- dios han existido antes de ser nombradas así. Recor- mente por el Ministerio de Cultura (campañas de foto- demos que no fue hasta 1973 cuando aparece este grafía, la llamada «Operación Escuelas», presencia de término y que su definición se debe a los expertos del colegios e institutos en el cine ), así como el Minis- Consejo Internacional del Cine y de la Televisión, que terio de la Juventud y Deportes que ha emprendido en el seno de la UNESCO, definen de esta forma: numerosas iniciativas. «Por educación en medios conviene entender el estu- Así, esta presencia de la educación en los medios dio, la enseñanza, el aprendizaje de los medios moder- no ha sido oficial. ¡La educación de los medios no apa- nos de comunicación y de expresión que forman parte rece oficialmente como tal en los textos de la escuela de un dominio específico y autónomo de conocimien- francesa hasta 2006! tos en la teoría y la práctica pedagógicas, a diferencia Este hecho no nos puede dejar de sorprender ya de su utilización como auxiliar para la enseñanza y el que las experiencias se han multiplicado desde el prin- aprendizaje en otros dominios de conocimientos tales Páginas 43-48 46 Comunicar, 28, 2007 como los de matemáticas, ciencias y geografía». A pe- mente en todas las asignaturas. Incluso los nuevos cu- sar de que esta definición ha servido para otorgarle un rrículos de materias científicas en 2006 para los alum- reconocimiento real, los debates sobre lo que abarca y nos de 11 a 18 años hacen referencia a la necesidad no, no están totalmente extinguidos. de trabajar sobre la información científica y técnica y En segundo lugar, porque si bien a la escuela fran- el uso de las imágenes que nacen de ella. cesa le gusta la innovación, después duda mucho en Desde junio de 2006, aparece oficialmente el tér- reflejar y sancionar estas prácticas innovadoras en sus mino «educación en medios» al publicar el Ministerio textos oficiales. Nos encontramos con una tradición de Educación los nuevos contenidos mínimos y las sólidamente fundada sobre una transmisión de conoci- competencias que deben adquirir los jóvenes al salir mientos muy estructurados, organizados en disciplinas del sistema educativo. escolares que se dedican la mayor parte a transmitir Este documento pretende averiguar cuáles son los conocimientos teóricos. La pedagogía es a menudo se- conocimientos y las competencias indispensables que cundaria, aunque los profesores disfrutan de una ver- deben dominar para terminar con éxito su escolaridad, dadera libertad pedagógica en sus clases. El trabajo seguir su formación y construir su futuro personal y crítico sobre los medios que estaba aún en elaboración profesional. Siete competencias diferentes han sido te- necesitaba este empuje para hacerse oficial. nidas en cuenta y en cada una de ellas, el trabajo con Aunque el trabajo de educación en los medios no los medios es reconocido frecuentemente. Para citar esté reconocido como disciplina, no está ausente de un ejemplo, la competencia sobre el dominio de la len- gua francesa definen las capa- cidades para expresarse oral- La metodología elaborada en el marco de la educación en mente que pueden adquirirse con la utilización de la radio e, medios parece incluso permitir la inclinación de la sociedad incluso, se propone fomentar de la información hacia una sociedad del conocimiento, como defiende la UNESCO. En Francia, se necesitaría unir el interés por la lectura a través de la lectura de la prensa. La educación en los medios las fuerzas dispersas en función de los soportes mediáticos y orientarse más hacia la educación en medios que al dominio adquiere pleno derecho y entidad en la sección sexta titulada «competencias sociales y cívi- técnico de los aparatos. cas» que indica que «los alum- nos deberán ser capaces de juz- gar y tendrán espíritu crítico, lo que supone ser educados en los las programaciones oficiales, ya que, a lo largo de un medios y tener conciencia de su lugar y de su influencia estudio de los textos, los documentalistas del CLEMI en la sociedad». han podido señalar más de una centena de referencias a la educación de los medios en el seno de disciplinas 4. Un entorno positivo como el francés, la historia, la geografía, las lenguas, Si nos atenemos a las cifras, el panorama de la las artes plásticas : trabajos sobre las portadas de educación en medios es muy positivo. Una gran ope- prensa, reflexiones sobre temas mediáticos, análisis de ración de visibilidad como la «Semana de la prensa y publicidad, análisis de imágenes desde todos los ángu- de los medios en la escuela», coordinada por el CLE- los, reflexión sobre las noticias en los países europeos, MI, confirma año tras año, después de 17 convocato- información y opinión rias, el atractivo que ejerce sobre los profesores y los Esta presencia se constata desde la escuela mater- alumnos. Concebida como una gran operación de nal (2 a 6 años) donde, por ejemplo, se le pregunta a complementariedad source of circulating FGF-21. The lack of association between circulating and muscle-expressed FGF-21 also suggests that muscle FGF-21 primarily works in a local manner regulating glucose metabolism in the muscle and/or signals to the adipose tissue in close contact to the muscle. Our study has some limitations. The number of subjects is small and some correlations could have been significant with greater statistical power. Another aspect is that protein levels of FGF-21 were not determined in the muscles extracts, consequently we cannot be sure the increase in FGF-21 mRNA is followed by increased protein expression. In conclusion, we show that FGF-21 mRNA is increased in skeletal muscle in HIV patients and that FGF-21 mRNA in muscle correlates to whole-body (primarily reflecting muscle) insulin resistance. These findings add to the evidence that FGF-21 is a myokine and that muscle FGF-21 might primarily work in an autocrine manner. Acknowledgments We thank the subjects for their participation in this study. Ruth Rousing, Hanne Willumsen, Carsten Nielsen and Flemming Jessen are thanked for excellent technical help. The Danish HIV-Cohort is thanked for providing us HIV-related data. 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(2010) Serum FGF21 levels are elevated in association with lipodystrophy, insulin resistance and biomarkers of liver injury in HIV-1-infected patients. AIDS 24: 2629–2637. PLOS ONE | www.plosone.org 7 March 2013 | Volume 8 | Issue 3 | e55632
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