Causes and consequences of variation in maternal effects in the wild

Lead Research Organisation: University of Edinburgh
Department Name: Sch of Biological Sciences

Abstract

Conditions experienced during early life can have large impacts on individual fitness. An important source of these early life effects is variation in pre- and postnatal maternal care - hence 'maternal effects', defined as the influence of a mother's phenotype on the phenotype of her offspring over and above the direct effect of genes inherited from her. Variation in maternal effects can be large, at least as large as that due to influences of the environment or of an individual's own genes. However, there are strikingly few investigations of these effects in natural as opposed to laboratory or farm populations and so their importance and evolutionary consequences have not been fully assessed; if these maternal effects are genetic in origin, they could be a major source of constraint in evolution.

In this study we will investigate the causes and consequences of maternal effects in the individually-monitored red deer of the Isle of Rum, Scotland. This is a particularly appropriate study population as males play no part in parental care, whilst females produce many calves over long lifetimes. Maternal effects on offspring traits are known to be large in this population; combined with complete pedigree information, high density genotyping data and life history data, this system is an excellent candidate for characterising the magnitude, direction and genomic location of maternal genetic effects on offspring phenotype.

Our aims are first, to estimate the variation in a range of traits such as birth weight and juvenile survival that is explained by different kinds of maternal effects: permanent environment effects such as those due to a mother's own rearing conditions and those due to additive genetic variation between mothers (i.e. genetic variation that can respond to directional selection). Second, we will determine the extent to which these maternal effects vary (interact) with the sex of the calf, the reproductive status of the mother, environmental conditions during pregnancy and the mother's age. Generally we expect maternal effects variance to increase as the investment required gets greater (sons more costly than daughters) or the conditions get tougher, but the reverse is also possible. Third, we will use new phenotypes obtained during the project for early milk quality, parasite load and antibody production, estimated non-invasively from faecal and neonatal blood samples, to investigate the extent to which we can explain the maternal effects documented earlier. Fourth, we will use genomic information to investigate the genomic location of maternal genetic effects, first by considering each chromosome in turn (chromosome partitioning), then by considering smaller regions of each chromosome (regional heritability, genome-wide association).

The final and ultimate aim of our proposal is to address a major puzzle in evolutionary research. In most cases where it has been measured, natural selection favours larger body size, and most body size traits are heritable, and yet species do not change body size over time. One hypothesis explaining this stasis is that there are constraints arising from the genetics of and selection on mothers. Thus, a mother's genes may affect offspring body size independently of the offspring's genes (maternal additive genetic effect) and there may be a negative genetic correlation between the maternal genetic effect and the offspring's own genetic effect on a trait. Whether this genetic correlation acts as an evolutionary constraint depends critically on the strength and direction of selection on both the offspring trait and maternal performance for this trait. We intend to measure all the parameters required to test the prediction of evolutionary constraint for the first time in a free-living population.

Planned Impact

Who will benefit?

We see two groupings of beneficiaries from the proposed research.

1) Wildlife managers.
2) The general public.

How will they benefit?

1) Wildlife managers: the management of abundant species involves many actions that are best based on understanding the basic biology of the species in question. Maternal effects have at least two important implications for wildlife managers. First they are likely to generate variation in the quality of offspring and recruitment to the breeding population. Hence populations will require regular monitoring and responsive management. Second, managers are often trying to select their populations e.g. in the case of deer, by shooting males judged to have small antlers for their age. Females are often culled unselectively, but demonstration of maternal effects may well suggest better strategies for selective culling of females.

2) The general public: The general public has a great appetite for understanding the behaviour, ecology and evolutionary outcomes we see in natural populations. By studying the genetic and selective regime of traits in the Rum deer we will help in the public understanding of constraint in evolution.

How will we engage with these groups?

1) Wildlife managers: At one level, we will aim to have impact at the scientific level by conventional publishing in journals with associated press releases and lay articles in wildlife management magazines. At a more practical level, we will attend events run by Scottish Natural Heritage (SNH), the Association of Deer Management Groups (ADMG) and other players in the deer management community which are designed to receive views from stakeholders, to deliver continuing professional development to deer managers and to bring scientists and stakeholders together. Depending on the findings of the study we will generate a new edition of our booklet 'Red deer research on the Isle of Rum NNR: management implications' published by SNH.

2) The general public. We intend to engage with and educate the general public by a wide range of methods including: on the Isle of Rum, by enhancing our documentation and presentations for visitors and continuing to assist TV crews filming in the study area - in particular we will try to get results from this study into TV story lines. Off-island we will continue with museum and science festival exhibits, press releases to attract media attention to our research and the project website and Twitter feed.

For a more detailed description please see the 'Pathways to Impact' document.

Publications

10 25 50
 
Description In red deer, we have estimated the influence of genetic differences between mothers on a range of characteristics of offspring. These maternal genetic effects are large for early life characteristics like birthweight and birth leg length, but as expected decline sharply for characteristics measured later in the offspring's life. For birth weight and birth leg length we have also tested whether offspring genes and maternal genes are in tension with each other or not - i.e. whether genetic variation causing a mother to have a large calf, when expressed in the calf, make it smaller or not. It turns out there is no genetic tie-up here. This means that the genetic architecture of birth body size does not constrain the evolution of birth body size.
Next we have investigated the levels of six different antibody types that are transferred via the colostrum in the blood of newborn deer calves. We have documented both variation between mothers, some of which is genetically-determined, and some environmentally-determined, and we have documented within-mother variation due to previous reproductive effort: rearing a calf in one year depresses colostrum antibodies the following year. Mothers that make more antibodies also give birth to heavier calves, but the antibodies do not appear to be important in explaining subsequent calf survival.
Exploitation Route Constraints due to maternal genetics effects are one of the potential explanations of evolutionary stasis. We have demonstrated that the genetic architecture of offspring traits does not constrain evolution in a species with extended maternal care.
Sectors Environment

 
Title Data from: Estimating selection on the act of inbreeding in a population with strong inbreeding depression 
Description Inbreeding depression is widely regarded as a driving force in the evolution of dispersal, mate choice and sperm selection. However, due to likely costs of inbreeding avoidance, which are poorly understood, it is unclear to what extent selection to avoid inbreeding is expected in nature. Moreover, there are currently very few empirical estimates of the strength of selection against the act of inbreeding (mating with a relative), as opposed to the fitness costs of being inbred. Here, we use data from the individual-based study of red deer on the Scottish island of Rum, a strongly polygynous system which harbours a large inbreeding load, to estimate selection against the act of inbreeding for each sex. We use pedigree and genomic estimates of relatedness between individuals and measure fitness using both lifetime breeding success (number of calves born) and lifetime reproductive success (number of calves surviving to independence), with the latter incorporating inbreeding depression in calf survival. We find for both sexes that the repeatability of the act of inbreeding was low (<0.1), suggesting little among-individual variation for this trait on which selection can act. Using the genomic measures there was significant selection against the act of inbreeding in males, but not in females, and there was considerable uncertainty in the estimate in both sexes. We discuss possible explanations for these patterns and their implications for understanding the evolution of inbreeding avoidance in natural populations. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
 
Title Fitness costs of parasites explain multiple life history tradeoffs in a wild mammal 
Description Reproduction in wild animals can divert limited resources away from immune defence, resulting in increased parasite burdens. A longstanding prediction of life history theory states that these parasites can harm the individual, reducing the organism's subsequent fitness and producing reproduction-fitness tradeoffs. Here, we examined associations among reproductive allocation, immunity, parasitism, and subsequent fitness in a wild population of individually identified red deer ( Cervus elaphus ). Using path analysis, we investigated whether costs of lactation for downstream survival and fecundity were mediated by changes in strongyle nematode count and mucosal antibody levels. Lactating females exhibited increased parasite counts, which were in turn associated with substantially decreased fitness in the following year in terms of overwinter survival, fecundity, subsequent calf weight, and parturition date. This study offers observational evidence for parasite regulation of multiple life history tradeoffs, supporting the role of parasites as an important mediating factor in wild mammal populations. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.n8pk0p2t7
 
Description 3 articles in German wildlife magazine 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Journalist Christian Holm and a colleague visited the field project during the 2018 calving season and subsequently published 3 magazine articles about the project in the German magazine 'Jager'.
Year(s) Of Engagement Activity 2018
 
Description Anglia Ruskin University visit 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Undergraduate students
Results and Impact Anglia Ruskin University Field Course visited the study area 13/10/19 and were given a briefing followed by Q & A and watched the rut from the visitor hide.
Year(s) Of Engagement Activity 2019
URL http://rumdeer.biology.ed.ac.uk/
 
Description Mallaig High School and Preston Lodge School visit 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact Visit on 6th-7th October 2018 by pupils of Mallaig High School and Preston Lodge School, Edinburgh, to conduct research projects on red deer, funded by a grant from the Royal Society (London) that pairs schools and research projects. Each student was involved in two projects: focal watches of male and female behaviour at the peak of the rut to compare activity budgets between the sexes, and measuring cast antlers to assess the relationship between antler size and breeding success. Presentation of results at the Royal Society in London in December 2018.
Year(s) Of Engagement Activity 2018
 
Description Moray House 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Moray House Centre for Sports and Excercise MSc course in Outdoor Education visited the study area 28/4/19 and were given a briefing followed by Q & A.
Year(s) Of Engagement Activity 2019
URL http://rumdeer.biology.ed.ac.uk/
 
Description Moray House (2nd group) 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Moray House Centre for Sports and Excercise MSc course in Outdoor Education (2nd group) visited the study area 4/5/19 and were given a briefing followed by Q & A.
Year(s) Of Engagement Activity 2019
URL http://rumdeer.biology.ed.ac.uk/
 
Description North Highland College visit 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Undergraduate students
Results and Impact North Highland College Game Keeping and Wildlife Management Course visited the study area 3/4/19 and were given a briefing followed by Q & A.
Year(s) Of Engagement Activity 2019
URL http://rumdeer.biology.ed.ac.uk/
 
Description Notting Hill Prep School visit 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact Notting Hill Prep School visited the study area 17/7/19 and were given a briefing followed by Q & A.
Year(s) Of Engagement Activity 2019
URL http://rumdeer.biology.ed.ac.uk/
 
Description Photo-essay in Guardian 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Guardian photographer Murdo MacLeod followed project workers for a week during the calving season and published an on-line photo essay
Year(s) Of Engagement Activity 2018
URL https://www.theguardian.com/environment/gallery/2018/jun/25/red-deer-isle-rum-scotland-in-pictures
 
Description Radio interview and newspaper articles 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact We made a press release about a new publication from the project which gives the first dissection of the mechanisms by which breeding dates (in this case calving dates) are advancing in a natural population, showing evidence for genetic change in breeding dates. Thsi generated a Radio Scotland Good Morning interview and several newspaper and website articles.
Year(s) Of Engagement Activity 2019
URL http://rumdeer.biology.ed.ac.uk/
 
Description Ranger Walk in calving - Isle of Rum Community Trust 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Isle of Rum Community Trust walk to see deer calves. Talk, observed animals, shown collection, discussion. Led by IRCT ranger and NERC assistant Ali Morris.
Year(s) Of Engagement Activity 2018
 
Description Ranger walk in the rut - Isle of Rum Community Trust 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Isle of Rum Community Trust walk to see the red deer rut. Talk, observed animals, shown collection, discussion. Led by IRCT ranger and NERC assistant Ali Morris.
Year(s) Of Engagement Activity 2018
 
Description University of Central Lancashire visit 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Undergraduate students
Results and Impact University of Central Lancashire field course visited the study area 22/5/19 and were given a briefing followed by Q & A.
Year(s) Of Engagement Activity 2019
URL http://rumdeer.biology.ed.ac.uk/