Maternal effects and evolution

1. Maternal effects and evolution Kate LessellsNetherlands Institute of Ecology

2. 1) Maternal effects Examples: Parental provisioning What is a maternal effect? Maternal effects are broadly defined as phenotypic variation in offspring that is a consequence of the mother’s phenotype rather than the genetic constitution of the offspring (Roff 1998)

3. 1) Maternal effects What is a maternal effect? Maternal effects are broadly defined as phenotypic variation in offspring that is a consequence of the mother’s phenotype rather than the genetic constitution of the offspring (Roff 1998) Examples: Coenagrion puella mothers with higher parasite loads produce larger larvae(Rolff 1999)

4. 1) Maternal effects What is a maternal effect? Maternal effects are broadly defined as phenotypic variation in offspring that is a consequence of the mother’s phenotype rather than the genetic constitution of the offspring (Roff 1998) Examples: Onthophagus taurus mothers mated to large-horned males provide more resources to their young(Kotiaho et al. 2003)

5. 1) Maternal effects What is a maternal effect? Maternal effects are broadly defined as phenotypic variation in offspring that is a consequence of the mother’s phenotype rather than the genetic constitution of the offspring (Roff 1998) Examples: Nest orientation by chestnut-collared longspurs affects chick growth(Lloyd & Martin 2004)

6. 1) Maternal effects NSF/NSERC/ESF workshop: Maternal effects NSF network: Integrating ecology and endocrinology in avian reproduction Maternal effects in birds involving hormones

7. 1) Maternal effects Maternal effects in birds involving hormones Maternal effects involve the mother “doing something” to the offspring – i.e. some maternal behaviour 1) Hormones control the maternal behaviour e.g. hormones control provisioning rates Evolutionary interest: Hormones might affect the outcome of evolution if they cause (rather than just modulating) trade-offs 2) Hormones are the maternal behaviour e.g. maternal yolk hormones Evolutionary interest: Understanding the action of the hormones in the light of evolutionary conflicts of interest

8. 1) Maternal effects Maternal genes Maternal environment Maternal phenotype Offspring phenotype

9. 1) Maternal effects Maternal genes Maternal environment Maternal phenotype StateInformation Behaviour Offspring phenotype

10. 1) Maternal effects Maternal genes Maternal environment Maternal phenotype Effects of maternal environment:- long-term: e.g. size- short-term: e.g. condition StateInformation Behaviour Offspring phenotype

11. 1) Maternal effects Maternal genes Maternal environment Maternal phenotype The maternal environment can also act as a cue, predicting the environment of the offspring StateInformation Behaviour Offspring phenotype

12. 1) Maternal effects Maternal genes Maternal environment Maternal phenotype Female “does something” that has an effect on the offspring’s phenotype StateInformation Behaviour Offspring phenotype

13. 1) Maternal effects Maternal genes Maternal environment Decision-making process Maternal phenotype - subject to selection, so expect the variation in offspring phenotype that the maternal effect brings about to be adaptive StateInformation Behaviour “Adaptive transgenerational phenotypic plasticity”(Mousseau & Fox 1998) Offspring phenotype - enables parents to translate their experience into adaptive variation in their offspring

14. 2) Adaptive transgenerational phenotypic plasticity Adaptive transgenerational phenotypic plasticity e.g. Rana arvalis – mother modifies jelly of her eggs in relation to pH to maximise embryo survival(Räsänen et al. 2003)

15. 2) Adaptive transgenerational phenotypic plasticity Transgenerational reaction norm: Offspring phenotype Maternal environment or behaviour Adaptive transgenerational phenotypic plasticity Maternal behaviour - and hence

16. 2) Adaptive transgenerational phenotypic plasticity Adaptive transgenerational phenotypic plasticity Transgenerational reaction norm: Maternal behaviour - and hence Offspring phenotype Maternal environment How to we determine what the optimal behaviour would be in each environment? – classical behavioural ecology approach – consider the costs and benefits

17. 2) Adaptive transgenerational phenotypic plasticity What maternal behaviour – and hence offspring phenotype – maximises mother’s fitness? Mother’s fitness = fitness through current offspring – “current fitness” - Wc + fitness through future offspring – “future fitness” - Wf Each of these components of fitness can be further split into: Benefit through current/future offspring – Bc/Bf Cost through current/future offspring – Cc/Cf Mother’s fitness = Wc + Wf = (Bc – Cc) + (Bf – Cf)

18. 2) Adaptive transgenerational phenotypic plasticity Current fitness Future fitness Mother’s fitness Bc = Wc Cf B, C or W W Wf Parental care Parental care Parental care Cc Bc B, C or W Wf W Wc Maternal behaviour Maternal behaviour Maternal behaviour Mother’s fitness = Wc + Wf = (Bc – Cc) + (Bf – Cf) Parental care: No future costs or benefits:

19. 2) Adaptive transgenerational phenotypic plasticity Bc Cf W Wc Bf B, C or W Cc Wf Maternal behaviour Maternal behaviour Maternal behaviour Mother’s fitness = Wc + Wf = (Bc – Cc) + (Bf – Cf) Current fitness Future fitness Mother’s fitness More generally: ● Need to take into account all costs and benefits to current and future fitness to understand adaptive maternal effects- so must measure these (experimentally)- need to know if effects on mother are divorced from effects on offspring (yolk hormones)

20. 2) Adaptive transgenerational phenotypic plasticity By repeating the analysis of costs and benefits in each possible environment, we can predict optimal maternal behaviour in each environment- build up the optimal transgenerational reaction norm: Maternal behaviour - and hence Offspring phenotype Maternal environment So is that it?

21. 3) Evolutionary conflicts of interest Evolutionary conflicts of interest: Family members tend to be related but – apart from identical twins and asexual clones – are never completely related As a result there are evolutionary conflicts of interest – what is best evolutionarily for one individual is not best evolutionarily for another individual

22. 3) Evolutionary conflicts of interest Parent-offspring conflict:- Parents are equally related to all offspring, but each offspring is more related to itself than to its current and future siblings-> Offspring are selected to be more selfish than their parent(s) are selected to be Sibling conflict:- Each offspring within a brood is more related to itself than its broodmates-> Offspring are selected to be (somewhat) selfish Sexual conflict (between parents):- Each parent pays the cost of only its own care, but gains fitness benefit from both it and its mate’s care-> Both parents are selected to leave/make other parent do more of the parental care Evolutionary conflicts of interest:

23. 3) Evolutionary conflicts of interest e.g. Begging behaviour- Offspring are selected to demand more than parents are selected to give - So who wins? So how are such conflicts of interest resolved? Ever-increasing exaggeration of need by offspring prevented by costs (energetic, predation) - Parent feeds its optimal amount- But fitness is reduced by costs of begging

24. 3) Evolutionary conflicts of interest ● ‘Rules’ will/may evolve Parental rule: how much to feed in relation to begging Chick rule: how much to beg in relation to hunger ● Selection between rules is reciprocal “Lying” by chicks selects parents to “downplay” response “Downplaying” by parents selects chicks to “lie” - Downplaying maybe selective if parents can predict when they will be lied to When signalling occurs between two individuals with an evolutionary conflict of interest, we should ask the questions:- why should the receiver pay any attention to the signal?- can the signaller get away with lying?

25. 3) Evolutionary conflicts of interest Maternal yolk hormones and evolutionary conflicts of interest Do evolutionary conflicts of interest make some of our explanations for yolk hormones difficult or untenable? Are yolk hormones a resource or a signal?

26. 3) Evolutionary conflicts of interest Current fitness Future fitness Mother’s fitness Bc Cf W Yolk T Wf Yolk T Yolk T Could yolk hormones be a resource?- by “resource” mean that yolk hormones are limiting: - have a direct positive effect on offspring fitness - are costly to mother to produce Unlike begging, no means for chicks to ‘demand’ more- mother could impose her own optimal distribution between eggs- could be an evolutionarily stable solution if yolk T is a resource ● But howdo they act as a resource? Why are they limiting?

27. 3) Evolutionary conflicts of interest Current fitness Future fitness Mother’s fitness Yolk T Yolk T Yolk T Cc Bc Wf W Wc Could yolk hormones be a signal?- by “signal” mean that yolk hormones carry information: - chicks can choose how they react to that information - not (necessarily) costly to mother to produce If there are no costs or benefits to future fitness, the mother’s optimum is the same as the chick’s optimum- i.e. there is no parent-offspring conflict - could be an evolutionarily stable solution if yolk T is a signal … BUT

28. 3) Evolutionary conflicts of interest Current fitness Future fitness Mother’s fitness Yolk T Yolk T Yolk T Cc Bc Wf W Wc ‘But’ 1) If parent is signalling availability of food to feed young- Chicks will increase food demand in response to yolk T- Thus there will be a cost to future fitness, and hence parent-offspring conflict - Parent can avoid the costs of conflict by adjusting its response to begging, rather than signalling to chick to adjust its begging in response to hunger - Parent should only signal current food availability if chick benefits from knowing in advance how much it will be fed – e.g. to adjust its target growth trajectory- For similar reasons, parents may signal expected feeding conditions for offspring once independent – may also ‘give away’ feeding conditions for provisioning parent if the two sets of feeding conditions are similar

29. 3) Evolutionary conflicts of interest Current fitness Future fitness Mother’s fitness Yolk T Yolk T Yolk T Cc Bc Wf W Wc ‘But’ 2) If there is more than one chick- So long as costs and benefits of response act individually on each chick, the offspring’s and mother’s optima are the same – signalling is evolutionarily stable- e.g. benefit of response is aggression reducing individual risk of kleptoparastism, and cost of response is immunosupression - But it will rarely be true that costs and benefits act individually- e.g.1 benefit of response is aggression used to defend a brood territory against kleptoparasitism by other chicks - will then be parent-offspring conflict over aggressiveness of chicks- e.g.2 parent might be signalling position in the laying sequence - will be parent-offspring conflict over how competitive each chick should be

30. 3) Evolutionary conflicts of interest ‘But’ 2) If there is more than one chick… If there is parent-offspring conflict (as in the examples), the chicks will modify their behaviour in response to the signal in a way that maximises their own fitness, not the mother’s- expect the mother to ‘lie’ – and the chicks to ‘downplay’ the signal- likely to be resolved in a way analagous to begging: - there will be unavoidable costs associated with the signal (either to mother or offspring) - the chicks will ‘win’, i.e. have their, not the mother’s optimal behaviour ● If yolk hormones are a signalling system, they are likely to carry unavoidable costs● Usage of information signalled should be consistent with the chick’s not the parent’s optimum- Rather paradoxically, the individual who has the information initially (the chicks know their hunger and signal it by begging; the mother knows the environmental conditions/laying order and signals it by yolk hormones) is not the one who achieves its optimum!

31. 3) Evolutionary conflicts of interest Could yolk hormones be a way for females to win in sexual conflict?- in essence, females might get the chicks to “lie” to the father about how hungry they are- e.g. in several species mothers put more androgen in eggs when mated to one year-old males - but father is expected to downplay this lying, in the same way that the mother would if the chicks lied to her as a result of parent-offspring conflict- similarly, fathers are expected to selectively downplay if they can predict when the mother would selectively make the chicks lie (as they would if the mother uses a paternal characteristic, such as age, to decide when to make the chicks lie)- therefore seems unlikely that females might manage to manipulate the male in this way

32. 4) Conclusions Conclusions: ● Maternal effects can be interpreted as adaptive transgenerational phenotypic plasticity that maximises the mother’s fitness ● However, care must be taken when there are evolutionary conflicts of interest, because the transgenerational reaction norm that maximises the mother’s fitness will not maximise the chick’s or father’s fitness- if the mother is providing a resource, she may be able to impose her own optimum- if she is signalling information, it may well be the chicks that can impose their optimum