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      Exploration of tissue-specific gene expression patterns underlying timing of breeding in contrasting temperature environments in a song bird

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          Abstract

          Background

          Seasonal timing of breeding is a life history trait with major fitness consequences but the genetic basis of the physiological mechanism underlying it, and how gene expression is affected by date and temperature, is not well known. In order to study this, we measured patterns of gene expression over different time points in three different tissues of the hypothalamic-pituitary-gonadal-liver axis, and investigated specifically how temperature affects this axis during breeding. We studied female great tits ( Parus major) from lines artificially selected for early and late timing of breeding that were housed in two contrasting temperature environments in climate-controlled aviaries. We collected hypothalamus, liver and ovary samples at three different time points (before and after onset of egg-laying). For each tissue, we sequenced whole transcriptomes of 12 pools ( n = 3 females) to analyse gene expression.

          Results

          Birds from the selection lines differed in expression especially for one gene with clear reproductive functions, zona pellucida glycoprotein 4 ( ZP4), which has also been shown to be under selection in these lines. Genes were differentially expressed at different time points in all tissues and most of the differentially expressed genes between the two temperature treatments were found in the liver. We identified a set of hub genes from all the tissues which showed high association to hormonal functions, suggesting that they have a core function in timing of breeding. We also found ample differentially expressed genes with largely unknown functions in birds.

          Conclusions

          We found differentially expressed genes associated with selection line and temperature treatment. Interestingly, the latter mainly in the liver suggesting that temperature effects on egg-laying date may happen down-stream in the physiological pathway. These findings, as well as our datasets, will further the knowledge of the mechanisms of tissue-specific avian seasonality in the future.

          Electronic supplementary material

          The online version of this article (10.1186/s12864-019-6043-0) contains supplementary material, which is available to authorized users.

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          Most cited references74

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          Keeping up with a warming world; assessing the rate of adaptation to climate change.

          The pivotal question in the debate on the ecological effects of climate change is whether species will be able to adapt fast enough to keep up with their changing environment. If we establish the maximal rate of adaptation, this will set an upper limit to the rate at which temperatures can increase without loss of biodiversity. The rate of adaptation will primarily be set by the rate of microevolution since (i) phenotypic plasticity alone is not sufficient as reaction norms will no longer be adaptive and hence microevolution on the reaction norm is needed, (ii) learning will be favourable to the individual but cannot be passed on to the next generations, (iii) maternal effects may play a role but, as with other forms of phenotypic plasticity, the response of offspring to the maternal cues will no longer be adaptive in a changing environment, and (iv) adaptation via immigration of individuals with genotypes adapted to warmer environments also involves microevolution as these genotypes are better adapted in terms of temperature, but not in terms of, for instance, photoperiod.Long-term studies on wild populations with individually known animals play an essential role in detecting and understanding the temporal trends in life-history traits, and to estimate the heritability of, and selection pressures on, life-history traits. However, additional measurements on other trophic levels and on the mechanisms underlying phenotypic plasticity are needed to predict the rate of microevolution, especially under changing conditions. Using this knowledge on heritability of, and selection on, life-history traits, in combination with climate scenarios, we will be able to predict the rate of adaptation for different climate scenarios. The final step is to use ecoevolutionary dynamical models to make the link to population viability and from there to biodiversity loss for those scenarios where the rate of adaptation is insufficient.
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            Warmer springs lead to mistimed reproduction in great tits (Parus major)

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              Climate change and unequal phenological changes across four trophic levels: constraints or adaptations?

              1. Climate change has been shown to affect the phenology of many organisms, but interestingly these shifts are often unequal across trophic levels, causing a mismatch between the phenology of organisms and their food. 2. We consider two alternative hypotheses: consumers are constrained to adjust sufficiently to the lower trophic level, or prey species react more strongly than their predators to reduce predation. We discuss both hypotheses with our analyses of changes in phenology across four trophic levels: tree budburst, peak biomass of herbivorous caterpillars, breeding phenology of four insectivorous bird species and an avian predator. 3. In our long-term study, we show that between 1988 and 2005, budburst advanced (not significantly) with 0.17 d yr(-1), while between 1985 and 2005 both caterpillars (0.75 d year(-1)) and the hatching date of the passerine species (range for four species: 0.36-0.50 d year(-1)) have advanced, whereas raptor hatching dates showed no trend. 4. The caterpillar peak date was closely correlated with budburst date, as were the passerine hatching dates with the peak caterpillar biomass date. In all these cases, however, the slopes were significantly less than unity, showing that the response of the consumers is weaker than that of their food. This was also true for the avian predator, for which hatching dates were not correlated with the peak availability of fledgling passerines. As a result, the match between food demand and availability deteriorated over time for both the passerines and the avian predators. 5. These results could equally well be explained by consumers' insufficient responses as a consequence of constraints in adapting to climate change, or by them trying to escape predation from a higher trophic level, or both. Selection on phenology could thus be both from matches of phenology with higher and lower levels, and quantifying these can shed new light on why some organisms do adjust their phenology to climate change, while others do not.
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                Author and article information

                Contributors
                V.Laine@nioo.knaw.nl
                I.Verhagen@nioo.knaw.nl
                C.Mateman@nioo.knaw.nl
                A.Pijl@nioo.knaw.nl
                tdwillia@sfu.ca
                P.Gienapp@nioo.knaw.nl
                K.vanOers@nioo.knaw.nl
                M.Visser@nioo.knaw.nl
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                2 September 2019
                2 September 2019
                2019
                : 20
                : 693
                Affiliations
                [1 ]ISNI 0000 0001 1013 0288, GRID grid.418375.c, Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), ; P.O. Box 50, 6700 AB Wageningen, The Netherlands
                [2 ]ISNI 0000 0004 1936 7494, GRID grid.61971.38, Department of Biological Sciences, , Simon Fraser University, ; Burnaby, Canada
                Author information
                http://orcid.org/0000-0002-4516-7002
                Article
                6043
                10.1186/s12864-019-6043-0
                6720064
                31477015
                2727f9be-2264-4a37-9a37-4e465a17eafe
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 1 May 2019
                : 19 August 2019
                Funding
                Funded by: ERC Advanced Grant
                Award ID: 339092
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Genetics
                transcriptomics,seasonal timing,aves,selection line
                Genetics
                transcriptomics, seasonal timing, aves, selection line

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