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      Maternal mRNA input of growth and stress-response-related genes in cichlids in relation to egg size and trophic specialization

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          Abstract

          Background

          Egg size represents an important form of maternal effect determined by a complex interplay of long-term adaptation and short-term plasticity balancing egg size with brood size. Haplochromine cichlids are maternal mouthbrooders showing differential parental investment in different species, manifested in great variation in egg size, brood size and duration of maternal care. Little is known about maternally determined molecular characters of eggs in fishes and their relation to egg size and trophic specialization. Here we investigate maternal mRNA inputs of selected growth- and stress-related genes in eggs of mouthbrooding cichlid fishes adapted to different trophic niches from Lake Tanganyika, Lake Malawi, Lake Victoria and compare them to their riverine allies.

          Results

          We first identified two reference genes, atf7ip and mid1ip1, to be suitable for cross-species quantification of mRNA abundance via qRT-PCR in the cichlid eggs. Using these reference genes, we found substantial variation in maternal mRNA input for a set of candidate genes related to growth and stress response across species and lakes. We observed negative correlation of mRNA abundance between two of growth hormone receptor paralogs ( ghr1 and ghr2) across all haplochromine cichlid species which also differentiate the species in the two younger lakes, Malawi and Lake Victoria, from those in Lake Tanganyika and ancestral riverine species. Furthermore, we found correlations between egg size and maternal mRNA abundance of two growth-related genes igf2 and ghr2 across the haplochromine cichlids as well as distinct clustering of the species based on their trophic specialization using maternal mRNA abundance of five genes ( ghr1, ghr2, igf2, gr and sgk1).

          Conclusions

          These findings indicate that variations in egg size in closely related cichlid species can be linked to differences in maternal RNA deposition of key growth-related genes. In addition, the cichlid species with contrasting trophic specialization deposit different levels of maternal mRNAs in their eggs for particular growth-related genes; however, it is unclear whether such differences contribute to differential morphogenesis at later stages of development. Our results provide first insights into this aspect of gene activation, as a basis for future studies targeting their role during ecomorphological specialization and adaptive radiation.

          Electronic supplementary material

          The online version of this article (10.1186/s13227-018-0112-3) contains supplementary material, which is available to authorized users.

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          Most cited references131

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          The adaptive significance of maternal effects

          T Mousseau (1998)
          Recently, the adaptive significance of maternal effects has been increasingly recognized. No longer are maternal effects relegated as simple `troublesome sources of environmental resemblance' that confound our ability to estimate accurately the genetic basis of traits of interest. Rather, it has become evident that many maternal effects have been shaped by the action of natural selection to act as a mechanism for adaptive phenotypic response to environmental heterogeneity. Consequently, maternal experience is translated into variation in offspring fitness.
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            Early development and fitness in birds and mammals.

            Conditions experienced during early development affect survival and reproductive performance in many bird and mammal species. Factors affecting early development can therefore have an important influence both on the optimization of life histories and on population dynamics. The understanding of these evolutionary and dynamic consequences is just starting to emerge.
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              The genomic substrate for adaptive radiation in African cichlid fish

              Cichlid fishes are famous for large, diverse and replicated adaptive radiations in the Great Lakes of East Africa. To understand the molecular mechanisms underlying cichlid phenotypic diversity, we sequenced the genomes and transcriptomes of five lineages of African cichlids: the Nile tilapia (Oreochromis niloticus), an ancestral lineage with low diversity; and four members of the East African lineage: Neolamprologus brichardi/pulcher (older radiation, Lake Tanganyika), Metriaclima zebra (recent radiation, Lake Malawi), Pundamilia nyererei (very recent radiation, Lake Victoria), and Astatotilapia burtoni (riverine species around Lake Tanganyika). We found an excess of gene duplications in the East African lineage compared to tilapia and other teleosts, an abundance of non-coding element divergence, accelerated coding sequence evolution, expression divergence associated with transposable element insertions, and regulation by novel microRNAs. In addition, we analysed sequence data from sixty individuals representing six closely related species from Lake Victoria, and show genome-wide diversifying selection on coding and regulatory variants, some of which were recruited from ancient polymorphisms. We conclude that a number of molecular mechanisms shaped East African cichlid genomes, and that amassing of standing variation during periods of relaxed purifying selection may have been important in facilitating subsequent evolutionary diversification.
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                Author and article information

                Contributors
                ehsanpashayahi@gmail.com
                pooja.singh09@gmail.com
                laurenelecaudey@gmail.com
                wolfgang.gessl@uni-graz.at
                christian.sturmbauer@uni-graz.at
                Journal
                EvoDevo
                Evodevo
                EvoDevo
                BioMed Central (London )
                2041-9139
                1 December 2018
                1 December 2018
                2018
                : 9
                : 23
                Affiliations
                [1 ]ISNI 0000000121539003, GRID grid.5110.5, Institute of Biology, , University of Graz, ; Universitätsplatz 2, 8010 Graz, Austria
                [2 ]ISNI 0000 0004 1936 9457, GRID grid.8993.b, Evolutionary Biology Centre, , Uppsala University, ; Norbyvägen 18A, 75236 Uppsala, Sweden
                Article
                112
                10.1186/s13227-018-0112-3
                6271631
                30519389
                5413664e-883e-4fe9-a9d4-5c646244e758
                © The Author(s) 2018

                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
                : 18 August 2018
                : 22 November 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100002428, Austrian Science Fund;
                Award ID: P22737
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Developmental biology
                haplochromine cichlids,maternal mrna,eggs,trophic specialization,adaptive radiation,east african lakes

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