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Evolutionary consequences of maternal effects and stress
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-7247-3742
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Maternal effects occur when maternal environment or phenotype influence offspring phenotype, in addition to genetic contribution of the mother. As maternal effects often influence phenotypes that are under natural selection, they hence have evolutionary consequences. Further, the expression of both maternal effects and evolutionary potential has been argued to depend on environmental conditions, but the evidence of this dependency for the process of adaptation has been inconclusive. The main objective of this thesis was to investigate evolutionary consequences of maternal effects and stressful or variable environmental conditions.

I started by performing a meta-analysis of quantitative genetic studies that investigated expression of additive genetic, maternal, and residual variance under both stressful and benign environmental conditions (Paper I). Data spanning over many animal taxa and stress types revealed that high levels of environmental stress correlated with increased expression of genetic and residual variances. However, against our predictions, maternal effects were relatively unaffected by stress.

In Paper II and III, I explored the evolutionary divergences of traits previously shown to be under maternal control. Specifically, in Paper II, I performed a second meta-analysis, that investigated if parents of common frogs (Rana temporaria) influenced offspring development time to mediate the effects of time constraints, across a latitudinal cline. I found that reproductive delay in the parental generation correlated with decreased development time in tadpoles of northern R. temporaria populations, suggesting that parental effects may further decrease development time in populations from time-constrained environments.

In Paper III, I used an annual killifish system, to explore if environmental unpredictability, measured by variation in precipitation during rainy season, correlated with maternally mediated variation in embryo development time (bet-hedging). Although I found significant among-species differences in variation in development time, there was no clear linear relationship between variation in development time and precipitation. The results suggest that either bet-hedging is not important for persistence in the unpredictable annual killifish habitats, or that other ecological factors, rather than precipitation unpredictability, influenced evolution of variation in development times.

Lastly, I investigated if occurrence of placenta correlated with increased offspring brain size among poeciliid fish (Paper IV). In contrast to our prediction, I did not find any consistent differences in relative brain size between the fry of placental and non-placental species. It is possible that either the poeciliid placental structures do not have a sufficient capacity to transfer resources necessary for increased brain development, or that other factors, such as sexual selection, or differences in food abundance and competition, shaped brain evolution among poeciliids.

In conclusion, the results of this thesis suggest that environmental stress may influence evolutionary potential by increasing genetic variation available for selection, that time-constrained habitats may be conducive to evolution of parental effects on offspring development times, and that maternal influence on offspring traits may be difficult to detect, as many ecological factors may potentially influence evolution of life-history and morphology traits.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2019. , p. 19
Keywords [en]
parental effects, meta-analysis, development time, bet-hedging, brain size, evolutionary potential, unpredictable environments
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-175589ISBN: 978-91-7797-907-4 (print)ISBN: 978-91-7797-908-1 (electronic)OAI: oai:DiVA.org:su-175589DiVA, id: diva2:1367840
Public defence
2019-12-20, Vivi Täckholmsalen (Q-salen) NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council, 2013-05064
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 2: Manuscript. Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2019-11-27 Created: 2019-11-05 Last updated: 2019-11-15Bibliographically approved
List of papers
1. Environmental stress correlates with increases in both genetic and residual variances: A meta-analysis of animal studies
Open this publication in new window or tab >>Environmental stress correlates with increases in both genetic and residual variances: A meta-analysis of animal studies
2017 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 71, no 5, p. 1339-1351Article in journal (Refereed) Published
Abstract [en]

Adaptive evolutionary responses are determined by the strength of selection and amount of genetic variation within traits, however, both are known to vary across environmental conditions. As selection is generally expected to be strongest under stressful conditions, understanding how the expression of genetic variation changes across stressful and benign environmental conditions is crucial for predicting the rate of adaptive change. Although theory generally predicts increased genetic variation under stress, previous syntheses of the field have found limited support for this notion. These studies have focused on heritability, which is dependent on other environmentally sensitive, but nongenetic, sources of variation. Here, we aim to complement these studies with a meta-analysis in which we examine changes in coefficient of variation (CV) in maternal, genetic, and residual variances across stressful and benign conditions. Confirming previous analyses, we did not find any clear direction in how heritability changes across stressful and benign conditions. However, when analyzing CV, we found higher genetic and residual variance under highly stressful conditions in life-history traits but not in morphological traits. Our findings are of broad significance to contemporary evolution suggesting that rapid evolutionary adaptive response may be mediated by increased evolutionary potential in stressed populations.

Keywords
Adaptation, genetic variation, heritability, life-history evolution, maternal effects, quantitative genetics
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-144706 (URN)10.1111/evo.13201 (DOI)000401256200017 ()28186615 (PubMedID)
Available from: 2017-07-21 Created: 2017-07-21 Last updated: 2019-11-05Bibliographically approved
2. Thermally induced parental effects influence life history traits and covary with an environmental cline in common frog populations
Open this publication in new window or tab >>Thermally induced parental effects influence life history traits and covary with an environmental cline in common frog populations
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Across latitudinal clines, the juvenile developmental rates of ectotherms often covary with the length of the growing season, due to life-history trade-offs imposed by time-constrained environments. However, as the start of the growing season often varies substantially across years, adaptive parental effects on juvenile developmental rates may mediate the costs of a delayed spring. By employing a meta-analysis, we tested whether larval developmental rates across a latitudinal cline of common frogs (Rana temporaria) are affected by fluctuating onsets of breeding, across years. We predicted that larval developmental rate will be inversely related to the onset of breeding, and that northern populations will be more prone to shorten their developmental rate in response to late breeding, as the costs of delayed metamorphosis should be highest in areas with a shorter growing season. We found that the larval period of both northern and southern populations responded to parental environmental conditions to similar degree in absolute terms, but in different directions. In northern populations, a late season start correlated with decreased development time, suggesting that the evolution of parental effects aid population persistence in time-constrained environments. In southern populations, late season start correlated with increased development time, which could potentially be explained as a predator avoidance strategy. Our findings suggest that local ecological variables can induce adaptive parental effects, but responses are complex, and likely trade-off with other ecological factors.

Keywords
maternal effects, phenology, local adaptation, temperature, trade-offs
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-175583 (URN)
Projects
Evolutionary consequences of maternal effects and stress
Funder
Swedish Research Council, 2013-05064
Note

This publication is under review.

Available from: 2019-11-05 Created: 2019-11-05 Last updated: 2019-12-09Bibliographically approved
3. Variation in developmental rates is not linked to environmental unpredictability in annual killifishes
Open this publication in new window or tab >>Variation in developmental rates is not linked to environmental unpredictability in annual killifishes
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Comparative evidence suggests that adaptive plasticity may evolve as a response to predictable environmental variation. However, receiving less attention is unpredictable environmental variation, which is considered to affect evolutionary trajectories by increasing phenotypic variation (bet-hedging). If increased variance in development time evolved as an adaptation to unpredictable environmental conditions, we would expect species inhabiting locations with unpredictable conditions to have a higher variance in development time. Here, we examine the occurrence of bet-hedging in egg developmental rate in seven species of annual killifish, originating from a gradient of precipitation rate variation, under three different incubation temperatures (21°C, 23°C, and 25°C). These fish species persist as dormant eggs buried in the soil, in seasonal environments with regular habitat desiccation. At the onset of the rainy season, the eggs must be sufficiently developed in order to hatch, and complete their life-cycle. We found substantial differences among species in both mean and variation of egg development rates, as well as species-specific plastic temperature responses. However, there was no clear relationship between variation in egg development time and variation in precipitation (environmental predictability). Hence, if species specific variances are adaptive, they do not diverge in accordance with simple linear relationship to variation in precipitation.

Keywords
bet hedging, diapause, development, maternal effects, plasticity, temperature response, ephemeral habitats
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-175586 (URN)
Projects
Evolutionary consequences of maternal effects and stress
Funder
Swedish Research Council, 2013-05064
Available from: 2019-11-05 Created: 2019-11-05 Last updated: 2019-12-09Bibliographically approved
4. The evolution of a placenta is not linked to increased brain size in poeciliid fishes
Open this publication in new window or tab >>The evolution of a placenta is not linked to increased brain size in poeciliid fishes
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Maternal investment traits are considered to have a direct influence on the size of energetically costly organs, including the brain. In placental organisms, offspring are supplied with nutrients during pre-natal development, which in turn may modulate brain size evolution. While this hypothesis has received some support in mammals (i.e. in the marsupial/placental transition), how the evolution of the placenta affects brain size in other taxa is largely unknown.Here, we use eight poeciliid fish species to test if species with placental transferred nutrients, invest more resources into offspring brain development than species with no placental structures. We predicted that the evolution of the placenta would be associated with larger relative brain size in fry, and possibly also shallower ontogenetic brain size allometry, if cognitive demands are similar in adults across placental and non-placental species. We tested these hypotheses by taking non-invasive brain size measurements during the first four weeks of life, and relating these to corresponding somatic growth. Contrary to our expectations, we did not find any differences in brain size between the two maternal strategies. Furthermore, we did not find any differences in how relative brain size changed over ontogenetic development between placental and non-placental species. Elsewhere, maternal investment traits have been commonly linked to brain size, however the species investigated here only exhibit pre-natal provisioning, which may reduce the potential for maternal investment into brain size. Our results suggest that coevolution between placental structures and juvenile brain size is not a general pattern.

Keywords
maternal provisioning, maternal effects, placenta, matrotrophy, expensive tissue, brain allometry, trade-offs
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-175588 (URN)
Projects
Evolutionary consequences of maternal effects and stress
Funder
Swedish Research Council, 2013-05064
Available from: 2019-11-05 Created: 2019-11-05 Last updated: 2019-12-09Bibliographically approved

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