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The evolution of a placenta is not linked to increased brain size in poeciliid fishes
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-7247-3742
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-3705-1907
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(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 [en]
maternal provisioning, maternal effects, placenta, matrotrophy, expensive tissue, brain allometry, trade-offs
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-175588OAI: oai:DiVA.org:su-175588DiVA, id: diva2:1367819
Projects
Evolutionary consequences of maternal effects and stress
Funder
Swedish Research Council, 2013-05064Available from: 2019-11-05 Created: 2019-11-05 Last updated: 2019-12-09Bibliographically approved
In thesis
1. Evolutionary consequences of maternal effects and stress
Open this publication in new window or tab >>Evolutionary consequences of maternal effects and stress
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
parental effects, meta-analysis, development time, bet-hedging, brain size, evolutionary potential, unpredictable environments
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-175589 (URN)978-91-7797-907-4 (ISBN)978-91-7797-908-1 (ISBN)
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

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Rowiński, PiotrNäslund, JoacimSowersby, WillEckerström-Liedholm, SimonRogell, Björn
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