scholarly journals Reproductive capacity evolves in response to ecology through common developmental mechanisms in Hawai’ian Drosophila

2018 ◽  
Author(s):  
Didem P. Sarikaya ◽  
Samuel H. Church ◽  
Laura P. Lagomarsino ◽  
Karl N. Magnacca ◽  
Steven Montgomery ◽  
...  

AbstractLifetime reproductive capacity, or the total number of offspring that an individual can give rise to in its lifetime, is a fitness component critical to the evolutionary process. In insects, female reproductive capacity is largely determined by the number of ovarioles, the egg-producing subunits of the ovary. Recent work has provided insights into the genetic and environmental control of ovariole number in Drosophila melanogaster. However, whether regulatory mechanisms discovered under laboratory conditions also explain evolutionary variation in natural populations is an outstanding question. Here we report, for the first time, insights into the mechanisms regulating ovariole number and its evolution among Hawai’ian Drosophila, a large adaptive radiation of fruit flies in which the highest and lowest ovariole numbers of the genus have evolved within 25 million years. Using phylogenetic comparative methods, we show that ovariole number variation among Hawai’ian Drosophila is best explained by adaptation to specific oviposition substrates. Further, we show that evolution of oviposition on ephemeral egg-laying substrates is linked to changes the allometric relationship between body size and ovariole number. Finally, we provide evidence that the developmental mechanism principally responsible for controlling ovariole number in D. melanogaster also regulates ovariole number in natural populations of Hawai’ian drosophilids. By integrating ecology, organismal growth, and cell behavior during development to understand the evolution of ovariole number, this work connects the ultimate and proximate mechanisms of evolutionary change in reproductive capacity.

2019 ◽  
Author(s):  
Tarun Kumar ◽  
Leo Blondel ◽  
Cassandra G. Extavour

AbstractUnderstanding the genetic regulation of organ structure is a fundamental problem in developmental biology. Here, we use egg-producing structures of insect ovaries, called ovarioles, to deduce systems-level gene regulatory relationships from quantitative functional genetic analysis. We previously showed that Hippo signalling, a conserved regulator of animal organ size, regulates ovariole number in Drosophila melanogaster. To comprehensively determine how Hippo signalling interacts with other pathways in this regulation, we screened all known signalling pathway genes, and identified Hpo-dependent and Hpo-independent signalling requirements. Network analysis of known protein-protein interactions among screen results identified independent gene regulatory sub-networks regulating one or both of ovariole number and egg laying. These sub-networks predict involvement of previously uncharacterised genes with higher accuracy than the original candidate screen. This shows that network analysis combining functional genetic and large-scale interaction data can predict function of novel genes regulating development.


1997 ◽  
Vol 69 (1) ◽  
pp. 17-23 ◽  
Author(s):  
SAMIA R'KHA ◽  
BRIGITTE MORETEAU ◽  
JERRY A. COYNE ◽  
JEAN R. DAVID

In the evolutionary process during which Drosophila sechellia became specialized on a toxic fruit (morinda), a spectacular decrease in female reproductive capacity took place when compared with the species' generalist relatives D. mauritiana and D. simulans. Comparisons of species and interspecific crosses showed that two different traits were modified: number of ovarioles and rate of egg production. During the conservation of a D. sechellia strain on usual food, adaptation to laboratory conditions led to an increase in the rate of oogenesis but not in ovariole number. Comparison of F1 and backcross progeny also suggests that the two traits are determined by different genes (ovariole number has already been shown to be polygenic). When morinda is available as a resource, the low rate of egg production in D. sechellia is partly compensated by a stimulating effect, while an inhibition occurs in D. simulans. It is assumed that D. sechellia progressively adapted itself from rotten, non-toxic morinda to a fresher and more toxic resource. During this process the rate of oogenesis evolved from an inhibition to a stimulation by morinda. Simultaneously a spectacular decrease in ovariole number took place, either as a consequence of stochastic events related to the small population size of D. sechellia and a metapopulation dynamics, or as an adaptive process favouring dispersal capacities of the female.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Tarun Kumar ◽  
Leo Blondel ◽  
Cassandra G Extavour

Understanding the genetic regulation of organ structure is a fundamental problem in developmental biology. Here, we use egg-producing structures of insect ovaries, called ovarioles, to deduce systems-level gene regulatory relationships from quantitative functional genetic analysis. We previously showed that Hippo signalling, a conserved regulator of animal organ size, regulates ovariole number in Drosophila melanogaster. To comprehensively determine how Hippo signalling interacts with other pathways in this regulation, we screened all known signalling pathway genes, and identified Hpo-dependent and Hpo-independent signalling requirements. Network analysis of known protein-protein interactions among screen results identified independent gene regulatory sub-networks regulating one or both of ovariole number and egg laying. These sub-networks predict involvement of previously uncharacterised genes with higher accuracy than the original candidate screen. This shows that network analysis combining functional genetic and large-scale interaction data can predict function of novel genes regulating development.


2017 ◽  
Vol 7 (7) ◽  
pp. 2391-2403 ◽  
Author(s):  
Amanda S Lobell ◽  
Rachel R Kaspari ◽  
Yazmin L Serrano Negron ◽  
Susan T Harbison

Abstract Ovariole number has a direct role in the number of eggs produced by an insect, suggesting that it is a key morphological fitness trait. Many studies have documented the variability of ovariole number and its relationship to other fitness and life-history traits in natural populations of Drosophila. However, the genes contributing to this variability are largely unknown. Here, we conducted a genome-wide association study of ovariole number in a natural population of flies. Using mutations and RNAi-mediated knockdown, we confirmed the effects of 24 candidate genes on ovariole number, including a novel gene, anneboleyn (formerly CG32000), that impacts both ovariole morphology and numbers of offspring produced. We also identified pleiotropic genes between ovariole number traits and sleep and activity behavior. While few polymorphisms overlapped between sleep parameters and ovariole number, 39 candidate genes were nevertheless in common. We verified the effects of seven genes on both ovariole number and sleep: bin3, blot, CG42389, kirre, slim, VAChT, and zfh1. Linkage disequilibrium among the polymorphisms in these common genes was low, suggesting that these polymorphisms may evolve independently.


Genetics ◽  
2001 ◽  
Vol 159 (4) ◽  
pp. 1415-1422 ◽  
Author(s):  
Sylvain Charlat ◽  
Claire Calmet ◽  
Hervé Merçot

Abstract Cytoplasmic incompatibility (CI) is induced by the endocellular bacterium Wolbachia. It results in an embryonic mortality occurring when infected males mate with uninfected females. The mechanism involved is currently unknown, but the mod resc model allows interpretation of all observations made so far. It postulates the existence of two bacterial functions: modification (mod) and rescue (resc). The mod function acts in the males' germline, before Wolbachia are shed from maturing sperm. If sperm is affected by mod, zygote development will fail unless resc is expressed in the egg. Interestingly, CI is also observed in crosses between infected males and infected females when the two partners bear different Wolbachia strains, demonstrating that mod and resc interact in a specific manner: Two Wolbachia strains are compatible with each other only if they harbor the same compatibility type. Here we focus on the evolutionary process involved in the emergence of new compatibility types from ancestral ones. We argue that new compatibility types are likely to evolve under a wider range of conditions than previously thought, through a two-step process. First, new mod variants can arise by mutation and spread by drift. This is possible because mod is expressed in males and Wolbachia is transmitted by females. Second, once such a mod variant achieves a certain frequency, it can create the conditions for the deterministic invasion of a new resc variant, allowing the invasion of a new mod resc pair. Furthermore, we show that a stable polymorphism might be maintained in natural populations, allowing the long-term existence of “suicidal” Wolbachia strains.


2021 ◽  
Vol 18 (1) ◽  
Author(s):  
Lucia Mentesana ◽  
Martin N. Andersson ◽  
Stefania Casagrande ◽  
Wolfgang Goymann ◽  
Caroline Isaksson ◽  
...  

Abstract Background In egg-laying animals, mothers can influence the developmental environment and thus the phenotype of their offspring by secreting various substances into the egg yolk. In birds, recent studies have demonstrated that different yolk substances can interactively affect offspring phenotype, but the implications of such effects for offspring fitness and phenotype in natural populations have remained unclear. We measured natural variation in the content of 31 yolk components known to shape offspring phenotypes including steroid hormones, antioxidants and fatty acids in eggs of free-living great tits (Parus major) during two breeding seasons. We tested for relationships between yolk component groupings and offspring fitness and phenotypes. Results Variation in hatchling and fledgling numbers was primarily explained by yolk fatty acids (including saturated, mono- and polyunsaturated fatty acids) - but not by androgen hormones and carotenoids, components previously considered to be major determinants of offspring phenotype. Fatty acids were also better predictors of variation in nestling oxidative status and size than androgens and carotenoids. Conclusions Our results suggest that fatty acids are important yolk substances that contribute to shaping offspring fitness and phenotype in free-living populations. Since polyunsaturated fatty acids cannot be produced de novo by the mother, but have to be obtained from the diet, these findings highlight potential mechanisms (e.g., weather, habitat quality, foraging ability) through which environmental variation may shape maternal effects and consequences for offspring. Our study represents an important first step towards unraveling interactive effects of multiple yolk substances on offspring fitness and phenotypes in free-living populations. It provides the basis for future experiments that will establish the pathways by which yolk components, singly and/or interactively, mediate maternal effects in natural populations.


2020 ◽  
Author(s):  
Melanie Lindner ◽  
Veronika N. Laine ◽  
Irene Verhagen ◽  
Heidi M. Viitaniemi ◽  
Marcel E. Visser ◽  
...  

ABSTRACTClimate change significantly impacts natural populations, particularly phenology traits, like the seasonal onset of reproduction in birds. This impact is mainly via plastic responses in phenology traits to changes in the environment, but the molecular mechanism mediating this plasticity remains elusive. Epigenetic modifications can mediate plasticity and consequently constitute promising candidates for mediating phenology traits. Here, we used genome-wide DNA methylation profiles of individual great tit (Parus major) females that we blood sampled repeatedly throughout the breeding season. We demonstrate rapid and directional variation in DNA methylation within the regulatory region of genes known to play key roles in avian reproduction that are in line with observed changes in gene expression in chickens. Our findings provide an important step towards unraveling the molecular mechanism mediating a key life history trait, an essential knowledge-gap for understanding how natural populations may cope with future climate change.IMPACT SUMMARYNatural populations are increasingly challenged by changing environmental conditions like global increases in temperature. A key way for species to adapt to global warming is via phenotypic plasticity, i.e. the ability to adjust the expression of traits to the environment. We, however, know little about how the environment can interact with an organism’s genetic make-up to shape its trait value. Epigenetic marks are known to vary with the environment and can modulate the expression of traits without any change in the genetic make-up and therefore have the potential to mediate phenotypic plasticity.To study the role of epigenetics for phenotypic plasticity, we here focus on the great tit (Parus major), a species that is strongly affected by global warming and plastic for temperature in an essential phenology trait, the seasonal onset of egg laying. As a first step, we investigated whether great tit females show within-individual and short-term variation in DNA methylation that corresponds to changes in the reproductive state of females. We therefore housed breeding pairs in climate-controlled aviaries to blood sample each female repeatedly throughout the breeding season and used these repeated samples for methylation profiling.We found rapid and directional variation in DNA methylation at the time females prepared to initiate egg laying that is located within the regulatory region of genes that have previously described functions for avian reproduction. Although future work is needed to establish a causal link between the observed temporal variation in DNA methylation and the onset of reproduction in female great tits, our work highlights the potential role for epigenetic modifications in mediating an essential phenology trait that is sensitive to temperatures.


2019 ◽  
Vol 22 (8) ◽  
pp. 1090-1096
Author(s):  
E. K. Karpova ◽  
I. Yu. Rauschenbach ◽  
N. E. Gruntenko

One of the crucial elements contributing to the adaptation of organisms to unfavorable environmental conditions is the reaction of stress. The study of its genetic control and role in adaptation to unfavorable conditions are of special interest. The juvenile hormone (JH) acts as a gonadotropic hormone in adult insects controlling the development of the ovaries, inducing vitellogenesis and oviposition. It was shown that a decrease in JH degradation in individuals reacting to adverse conditions by stress reaction (R­individuals) causes delay in egg laying and seems to allow the population to “wait out” the unfavorable conditions, thereby contributing to the adaptation at the population level. However, monitoring natural populations of D. melanogaster for the capability of stress reaction demonstrated that they have a high percentage of individuals incapable of it (NR­individuals). The study of reproductive characteristics of R­ and NR­individuals showed that under normal conditions R­individuals have the advantage of procreating offspring. Under unfavorable conditions, if the stressor is intense enough, NR­individuals die, but if its intensity is low, then they, unlike R­individuals, continue to produce offspring. Based on these data, it was hypothesized that the balance of R­ and NR­alleles in the population ensures its adaptation under frequent stresses of low intensity. To verify the hypothesis by an experiment, the ftness characteristics (lifespan, fecundity) of the R and NR lines of D. virilis were studied under normal conditions and under regular heat stress of various frequency.


2013 ◽  
Vol 280 (1751) ◽  
pp. 20122387 ◽  
Author(s):  
Jan Suda ◽  
Tomáš Herben

Genome duplication (polyploidy) is a recurrent evolutionary process in plants, often conferring instant reproductive isolation and thus potentially leading to speciation. Outcome of the process is often seen in the field as different cytotypes co-occur in many plant populations. Failure of meiotic reduction during gametogenesis is widely acknowledged to be the main mode of polyploid formation. To get insight into its role in the dynamics of polyploidy generation under natural conditions, and coexistence of several ploidy levels, we developed a general gametic model for diploid–polyploid systems. This model predicts equilibrium ploidy frequencies as functions of several parameters, namely the unreduced gamete proportions and fertilities of higher ploidy plants. We used data on field ploidy frequencies for 39 presumably autopolyploid plant species/populations to infer numerical values of the model parameters (either analytically or using an optimization procedure). With the exception of a few species, the model fit was very high. The estimated proportions of unreduced gametes (median of 0.0089) matched published estimates well. Our results imply that conditions for cytotype coexistence in natural populations are likely to be less restrictive than previously assumed. In addition, rather simple models show sufficiently rich behaviour to explain the prevalence of polyploids among flowering plants.


2015 ◽  
Vol 106 (2) ◽  
pp. 154-160 ◽  
Author(s):  
Y. Wu ◽  
F. Li ◽  
Z. Li ◽  
V. Stejskal ◽  
Z. Kučerová ◽  
...  

AbstractCryptolestes ferrugineus (Stephens, 1831) is an important insect pest of stored products. Due to its broad host range, short life cycle, and high reproductive capacity, this species has rapidly colonized temperate and tropical regions around the world. In this study, we isolated 18 novel polymorphic microsatellite loci from an enriched genomic library based on a biotin/streptavidin capture protocol. These loci will be useful tool to better understand the genetic structure and migration patterns of C. ferrugineus throughout the world. The genetic parameters were estimated based on 80 individual C. ferrugineus from two natural populations. The results revealed that 18 loci were different polymorphic levels. The numbers of alleles ranged from 3 to 12, and eleven loci demonstrated polymorphic information contents greater than 0.5. The observed (HO) and expected (HE) heterozygosities ranged from 0.051 to 0.883 and 0.173 to 0.815, respectively. Five locus/population combinations significantly deviated from Hardy–Weinberg equilibrium. We also demonstrated the potential utility of the C. ferrugineus microsatellites as population and species markers for four additional Cryptolestes species.


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