Literature DB >> 16321782

Poor maternal environment enhances offspring disease resistance in an invertebrate.

Suzanne E Mitchell1, Andrew F Read.   

Abstract

Natural populations vary tremendously in their susceptibility to infectious disease agents. The factors (environmental or genetic) that underlie this variation determine the impact of disease on host population dynamics and evolution, and affect our capacity to contain disease outbreaks and to enhance resistance in agricultural animals and disease vectors. Here, we show that changes in the environmental conditions under which female Daphnia magna are kept can more than halve the susceptibility of their offspring to bacterial infection. Counter-intuitively, and unlike the effects typically observed in vertebrates for transfer of immunity, mothers producing offspring under poor conditions produced more resistant offspring than did mothers producing offspring in favourable conditions. This effect occurred when mothers who were well provisioned during their own development then found themselves reproducing in poor conditions. These effects likely reflect adaptive optimal resource allocation where better quality offspring are produced in poor environments to enhance survival. Maternal exposure to parasites also reduced offspring susceptibility, depending on host genotype and offspring food levels. These maternal responses to environmental conditions mean that studies focused on a single generation, and those in which environmental variation is experimentally minimized, may fail to describe the crucial parameters that influence the spread of disease. The large maternal effects we report here will, if they are widespread in nature, affect disease dynamics, the level of genetic polymorphism in populations, and likely weaken the evolutionary response to parasite-mediated selection.

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Year:  2005        PMID: 16321782      PMCID: PMC1559984          DOI: 10.1098/rspb.2005.3253

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  12 in total

1.  Modelling density-dependent resistance in insect-pathogen interactions.

Authors:  K A White; K Wilson
Journal:  Theor Popul Biol       Date:  1999-10       Impact factor: 1.570

2.  Maternal control of resting-egg production in Daphnia.

Authors:  V Alekseev; W Lampert
Journal:  Nature       Date:  2001 Dec 20-27       Impact factor: 49.962

Review 3.  Biological and biomedical implications of the co-evolution of pathogens and their hosts.

Authors:  Mark E J Woolhouse; Joanne P Webster; Esteban Domingo; Brian Charlesworth; Bruce R Levin
Journal:  Nat Genet       Date:  2002-12       Impact factor: 38.330

Review 4.  Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission.

Authors:  Jennifer L Grindstaff; Edmund D Brodie; Ellen D Ketterson
Journal:  Proc Biol Sci       Date:  2003-11-22       Impact factor: 5.349

5.  Maternal transfer of strain-specific immunity in an invertebrate.

Authors:  Tom J Little; Benjamin O'Connor; Nick Colegrave; Kathryn Watt; Andrew F Read
Journal:  Curr Biol       Date:  2003-03-18       Impact factor: 10.834

6.  Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen.

Authors:  Suzanne E Mitchell; Emily S Rogers; Tom J Little; Andrew F Read
Journal:  Evolution       Date:  2005-01       Impact factor: 3.694

7.  Maternal transmission of immunity to white spot syndrome associated virus (WSSV) in shrimp (Penaeus monodon).

Authors:  C C Huang; Y L Song
Journal:  Dev Comp Immunol       Date:  1999 Oct-Dec       Impact factor: 3.636

8.  Egg investment is influenced by male attractiveness in the mallard.

Authors:  E J Cunningham; A F Russell
Journal:  Nature       Date:  2000-03-02       Impact factor: 49.962

9.  Testing small clutch size models with Daphnia.

Authors:  Meghan A Guinnee; Stuart A West; Tom J Little
Journal:  Am Nat       Date:  2004-05-20       Impact factor: 3.926

10.  Resource availability, maternal effects, and longevity.

Authors:  M Lynch; R Ennis
Journal:  Exp Gerontol       Date:  1983       Impact factor: 4.032

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  36 in total

Review 1.  Embryo stability and vulnerability in an always changing world.

Authors:  Amro Hamdoun; David Epel
Journal:  Proc Natl Acad Sci U S A       Date:  2007-01-30       Impact factor: 11.205

2.  Maternal effects on phenotypic plasticity in larvae of the salamander Hynobius retardatus.

Authors:  Hirofumi Michimae; Kinya Nishimura; Yoichiro Tamori; Masami Wakahara
Journal:  Oecologia       Date:  2009-04-08       Impact factor: 3.225

3.  Mothers produce less aggressive sons with altered immunity when there is a threat of disease during pregnancy.

Authors:  Olivia Curno; Jerzy M Behnke; Alan G McElligott; Tom Reader; Chris J Barnard
Journal:  Proc Biol Sci       Date:  2009-03-22       Impact factor: 5.349

Review 4.  Immunity in a variable world.

Authors:  Brian P Lazzaro; Tom J Little
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2009-01-12       Impact factor: 6.237

5.  Disentangling the influence of parasite genotype, host genotype and maternal environment on different stages of bacterial infection in Daphnia magna.

Authors:  Matthew D Hall; Dieter Ebert
Journal:  Proc Biol Sci       Date:  2012-05-16       Impact factor: 5.349

6.  Transgenerational effects of poor elemental food quality on Daphnia magna.

Authors:  Paul C Frost; Dieter Ebert; James H Larson; Michelle A Marcus; Nicole D Wagner; Alexandra Zalewski
Journal:  Oecologia       Date:  2009-12-02       Impact factor: 3.225

Review 7.  Recent advances in vertebrate and invertebrate transgenerational immunity in the light of ecology and evolution.

Authors:  Olivia Roth; Anne Beemelmanns; Seth M Barribeau; Ben M Sadd
Journal:  Heredity (Edinb)       Date:  2018-06-18       Impact factor: 3.821

8.  Transgenerational effect of infection in Plasmodium-infected mosquitoes.

Authors:  R Pigeault; J Vézilier; A Nicot; S Gandon; A Rivero
Journal:  Biol Lett       Date:  2015-03       Impact factor: 3.703

9.  Inter-annual variation in prevalence and intensity of mite parasitism relates to appearance and expression of damselfly resistance.

Authors:  Laura Nagel; Tonia Robb; Mark R Forbes
Journal:  BMC Ecol       Date:  2010-02-14       Impact factor: 2.964

10.  Successfully resisting a pathogen is rarely costly in Daphnia magna.

Authors:  Pierrick Labbé; Pedro F Vale; Tom J Little
Journal:  BMC Evol Biol       Date:  2010-11-17       Impact factor: 3.260

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