Adaptation to temporally fluctuating environments by the evolution of maternal effects

Most organisms live in ever-challenging temporally fluctuating environments. Theory suggests that the evolution of anticipatory (or deterministic) maternal effects underlies adaptation to environments that regularly fluctuate every other generation because of selection for increased offspring performance. Evolution of maternal bet-hedging reproductive strategies that randomize offspring phenotypes is in turn expected to underlie adaptation to irregularly fluctuating environments. Although maternal effects are ubiquitous their adaptive significance is unknown since they can easily evolve as a correlated response to selection for increased maternal performance. Using the nematode Caenorhabditis elegans, we show the experimental evolution of maternal provisioning of offspring with glycogen, in populations facing a novel anoxia hatching environment every other generation. As expected with the evolution of deterministic maternal effects, improved embryo hatching survival under anoxia evolved at the expense of fecundity and glycogen provisioning when mothers experienced anoxia early in life. Unexpectedly, populations facing an irregularly fluctuating anoxia hatching environment failed to evolve maternal bet-hedging reproductive strategies. Instead, adaptation in these populations should have occurred through the evolution of balancing trade-offs over multiple generations, since they evolved reduced fitness over successive generations in anoxia but did not go extinct during experimental evolution. Mathematical modelling confirms our conclusion that adaptation to a wide range of patterns of environmental fluctuations hinges on the existence of deterministic maternal effects, and that they are generally much more likely to contribute to adaptation than maternal bet-hedging reproductive strategies.

Download Full-text

Selection and niche trade-offs in biofilm-forming bacterial communities in experimental microcosms

Access Microbiology ◽

10.1099/acmi.ac2020.po0225 ◽

2020 ◽

Vol 2 (7A) ◽

Author(s):

Robyn Jerdan ◽

Scott Cameron ◽

Emily Donaldson ◽

Andrew Spiers

Keyword(s):

Biofilm Formation ◽

Liquid Column ◽

Significant Shift ◽

Bet Hedging ◽

Transfer Experiment ◽

Serial Transfer ◽

Fitness Advantage ◽

Trade Offs ◽

Selection For ◽

Cell Densities

Static microcosms are a well-established system used to study the adaptive radiation of Pseudomonas fluorescens SBW25 and the adaptive biofilm-forming mutants known as the Wrinkly Spreaders (WS). We have developed this system to investigate selection within multi-species communities using a soil-wash inoculum dominated by biofilm-competent pseudomonads. Here we present community and isolate-level analyses of one serial-transfer experiment in which replicate populations were selected for over ten transfers and 60 days. Although no significant trends in improving community biofilm characteristics or total microcosm productivity were observed, a significant shift in biofilm-formation and microcosm growth by individual isolates recovered from the initial soil-wash inoculum and final transfers indicated that these communities were subject to selection for growth in these microcosms. Surprisingly, the fitness of the archetypal WS was poor when competing against community samples, and having compared the cell densities in the low-O2 region of liquid column below the biofilm, we suggest that part of the community’s fitness advantage comes from the ability to colonise this under-utilised niche as well as to compete at the A-L interface. Samples from the community biofilms and the low-O2 region were able to re-colonize both niches and many final transfer isolates grew throughout the liquid column as well as forming A-L interface biofilms. This suggests that there is a trade-off between fast growth under highly competitive conditions at the A-L interface and slower growth with less competition in the low-O2 region, with some isolates taking a bet-hedging approach a colonizing both niches in our microcosm system.

Download Full-text

What kind of maternal effects are selected for in fluctuating environments?

10.1101/034546 ◽

2015 ◽

Cited By ~ 1

Author(s):

Stephen R Proulx ◽

Henrique Teotonio

Keyword(s):

Maternal Effects ◽

Developmental Plasticity ◽

Ancestral State ◽

Bet Hedging ◽

Alternative Phenotypes ◽

Fluctuating Environments ◽

Small Set ◽

The One ◽

Maternal Strategy

Adaptation to temporally fluctuating environments can be achieved through direct phenotypic evolution, by phenotypic plasticity (either developmental plasticity or trans-generational plasticity), or by randomizing offspring phenotypes (often called diversifying bet-hedging). Theory has long held that plasticity can evolve when information about the future environment is reliable while bet-hedging can evolve when mixtures of phenotypes have high average fitness (leading to low among generation variance in fitness). To date, no study has studied the evolutionary routes that lead to the evolution of randomized offspring phenotypes on the one hand or deterministic maternal effects on the other. We develop simple, yet general, models of the evolution of maternal effects and are able to directly compare selection for deterministic and randomizing maternal effects and can also incorporate the notion of differential maternal costs of producing offspring with alternative phenotypes. We find that only a small set of parameters allow bet hedging type strategies to outcompete deterministic maternal effects. Not only must there be little or no informative cues available, but also the frequency with which different environments are present must fall within a narrow range. By contrast, when we consider the joint evolution of the maternal strategy and the set of offspring phenotypes we find that deterministic maternal effects can always invade the ancestral state (lacking any form of maternal effect). The long-term ESS may, however, involve some form of offspring randomization, but only if the phenotypes evolve extreme differences in environment-specific fitness. Overall we conclude that deterministic maternal effects are much more likely to evolve than offspring randomization, and offspring randomization will only be maintained if it results in extreme differences in environment-specific fitness.

Download Full-text

Uterine and Postnatal Maternal Effects in Mice Selected for Differential Rate of Early Development

Genetics ◽

10.1093/genetics/153.2.905 ◽

1999 ◽

Vol 153 (2) ◽

pp. 905-917 ◽

Cited By ~ 1

Author(s):

Brian K Rhees ◽

Cynthia A Ernst ◽

Christina H Miao ◽

William R Atchley

Keyword(s):

Postnatal Development ◽

Maternal Effects ◽

Tail Length ◽

Postnatal Growth ◽

Correlated Response ◽

Control Line ◽

Differential Rate ◽

Early Postnatal Development ◽

Specific Effects ◽

Selection For

Abstract A series of mouse lines was produced by long-term restricted index selection for divergent rate of growth during early and late postnatal development. The selection program was based on the following treatments: E+ and E- lines were selected to alter birth to 10-day weight gain while holding late gain for both lines constant and a control line was established via random selection. Using embryo transfer and crossfostering methodology, we partitioned postnatal growth for E+, E-, and C lines into progeny genetic, uterine maternal, and nurse maternal components. Selection for differential early growth resulted in correlated response in uterine and nurse maternal effects on body weights, with significant genetic-by-environment interactions. Significant uterine effects were also observed in tail length measurements. Direct uterine effects on body weight were relatively small and resulted in growth rate differences early in development. Nurse effects were large, resulting in modification of progeny growth trajectory especially during early postnatal development. Genetic-by-uterine interactions were large and demonstrate progeny-specific effects of the prenatal uterine environment.

Download Full-text

Division of labor, bet hedging, and the evolution of mixed biofilm investment strategies

10.1101/107102 ◽

2017 ◽

Author(s):

Nick Vallespir Lowery ◽

Luke McNally ◽

William C. Ratcliff ◽

Sam P. Brown

Keyword(s):

Division Of Labor ◽

Experimental Evolution ◽

Cost Effective ◽

Investment Strategies ◽

Bacterial Cells ◽

Bet Hedging ◽

Planktonic Cells ◽

Selection For ◽

Experimental Findings ◽

Slow Growing

ABSTRACTBacterial cells, like many other organisms, face a tradeoff between longevity and fecundity. Planktonic cells are fast growing and fragile, while biofilm cells are often slower growing but stress resistant. Here we ask: why do bacterial lineages invest simultaneously in both fast and slow growing types? We develop a population dynamical model of lineage expansion across a patchy environment, and find that mixed investment is favored across a broad range of environmental conditions, even when transmission is entirely via biofilm cells. This mixed strategy is favored because of a division of labor, where exponentially dividing planktonic cells can act as an engine for the production of future biofilm cells, which grow more slowly. We use experimental evolution to test our predictions, and show that phenotypic heterogeneity is persistent even under selection for purely planktonic or purely biofilm transmission. Furthermore, simulations suggest that maintenance of a biofilm subpopulation serves as a cost-effective hedge against environmental uncertainty, which is also consistent with our experimental findings.

Download Full-text

Genetic parameters of growth traits in Nellore cattle

Semina Ciências Agrárias ◽

10.5433/1679-0359.2017v38n3p1503 ◽

2017 ◽

Vol 38 (3) ◽

pp. 1513

Author(s):

Leandro Molina Kamei ◽

Edson Luis De Azambuja Ribeiro ◽

Nilva Aparecida Nicolao Fonseca ◽

Carolina Amália De Souza Dantas Muniz ◽

Tatiane Vito Camiloti ◽

...

Keyword(s):

Genetic Correlation ◽

Maternal Effects ◽

Fixed Effects ◽

Growth Traits ◽

Correlation Coefficients ◽

Correlated Response ◽

Environmental Correlations ◽

Nellore Cattle ◽

Selection For ◽

Heritability Estimates

This study evaluated non-genetic factors and calculated heritability estimates of direct and maternal effects for growth traits in Nellore cattle raised in southern Brazil. Performance records of 4170, 1538, 3139, 1830, and 1151 calves born from 2005 to 2011 were analyzed for birth weight (BW), adjusted120-day weight (W120), adjusted 205-day weight (W205), adjusted365-day weight (W365), and adjusted 550-day weight (W550), respectively. The components of (co)variance used to calculate heritability estimates were determined by Derivative-Free Restricted Maximum Likelihood using the MTDFREML software. Contemporary groups were included in the model as fixed effects, and direct and maternal effects, permanent environmental effects, and residual errors were included as random effects. Phenotypic correlations were estimated using the PROC CORR procedure from SAS. Overall means for BW, W120, W205, W365, and W550 were 38, 138, 201, 270, and 376 kg, respectively. Heritability estimates for direct and maternal effects were 0.17 ± 0.04 and 0.11 ± 0.03 (BW), 0.14 ± 0.03 and 0.03 ± 0.04 (W120), and 0.17 ± 0.04 and 0.09 ± 0.03 (W205). Genetic, phenotypic, and environmental correlations were 0.79, 0.44, and 0.32 for BW and W120, 0.79, 0.39, and 0.26 for BW and W205, and 0.96, 0.74, and 0.75 for W120 and W205. The results indicate that selection for pre-weaning weight would be more efficient using W205, and genetic correlation coefficients indicate that selection at any age should produce a positively correlated response at older ages. Genetic, phenotypic, and environmental correlation coefficients between W365 and W550 were 0.99, 0.75, and 0.76, respectively. Selection for adjusted 550-day weight should produce the greatest genetic gains. Genetic correlation coefficients between weight traits indicate that selection for weight at older ages, which could help reduce the number of weighings and increase accuracy of selection at younger ages, produces gains at older ages.

Download Full-text

Evolution of maternal effect senescence

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1520494113 ◽

2015 ◽

Vol 113 (2) ◽

pp. 362-367 ◽

Cited By ~ 28

Author(s):

Jacob A. Moorad ◽

Daniel H. Nussey

Keyword(s):

Maternal Effects ◽

Maternal Effect ◽

Genetic Model ◽

Theoretical Perspective ◽

Evolutionary Model ◽

Social Contexts ◽

Offspring Performance ◽

The Social ◽

Quantitative Genetic Model ◽

Selection For

Increased maternal age at reproduction is often associated with decreased offspring performance in numerous species of plants and animals (including humans). Current evolutionary theory considers such maternal effect senescence as part of a unified process of reproductive senescence, which is under identical age-specific selective pressures to fertility. We offer a novel theoretical perspective by combining William Hamilton’s evolutionary model for aging with a quantitative genetic model of indirect genetic effects. We demonstrate that fertility and maternal effect senescence are likely to experience different patterns of age-specific selection and thus can evolve to take divergent forms. Applied to neonatal survival, we find that selection for maternal effects is the product of age-specific fertility and Hamilton’s age-specific force of selection for fertility. Population genetic models show that senescence for these maternal effects can evolve in the absence of reproductive or actuarial senescence; this implies that maternal effect aging is a fundamentally distinct demographic manifestation of the evolution of aging. However, brief periods of increasingly beneficial maternal effects can evolve when fertility increases with age faster than cumulative survival declines. This is most likely to occur early in life. Our integration of theory provides a general framework with which to model, measure, and compare the evolutionary determinants of the social manifestations of aging. Extension of our maternal effects model to other ecological and social contexts could provide important insights into the drivers of the astonishing diversity of lifespans and aging patterns observed among species.

Download Full-text

Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys

10.1101/2021.01.28.428572 ◽

2021 ◽

Author(s):

Arunas L. Radzvilavicius ◽

Iain G. Johnston

Keyword(s):

General Theory ◽

Bet Hedging ◽

Beneficial Mutations ◽

Environmental Challenges ◽

Organelle Dna ◽

Fluctuating Environments ◽

Cellular Bioenergetics ◽

Selection For ◽

Evolutionary Simulations ◽

New Mutations

AbstractBioenergetic organelles – mitochondria and plastids – retain their own genomes, and these organelle DNA (oDNA) molecules are vital for eukaryotic life. Like all genomes, oDNA must be able to evolve to suit new environmental challenges. However, mixed oDNA populations can challenge cellular bioenergetics, providing a penalty to the appearance and adaptation of new mutations. Here we show that organelle ‘bottlenecks’, mechanisms increasing cell-to-cell oDNA variability during development, can overcome this mixture penalty and facilitate the adaptation of beneficial mutations. We show that oDNA heteroplasmy and bottlenecks naturally emerge in evolutionary simulations subjected to fluctuating environments, demonstrating that this evolvability is itself evolvable. Usually thought of as a mechanism to clear damaging mutations, organelle bottlenecks therefore also resolve the tension between intracellular selection for pure oDNA populations and the ‘bet-hedging’ need for evolvability and adaptation to new environments. This general theory suggests a reason for the maintenance of organelle heteroplasmy in cells, and may explain some of the observed diversity in organelle maintenance and inheritance across taxa.

Download Full-text