Amphibians with infectious disease increase their reproductive effort: evidence for the terminal investment hypothesis

Mounting an immune response to fight disease is costly for an organism and can reduce investment in another life-history trait, such as reproduction. The terminal investment hypothesis predicts that an organism will increase reproductive effort when threatened by disease. The reproductive fitness of amphibians infected with the deadly fungal pathogen Batrachochytrium dendrobatidis ( Bd ) is largely unknown. In this study, we explored gametogenesis in two endangered and susceptible frog species, Pseudophryne corroboree and Litoria verreauxii alpina. Gametogenesis, both oogenesis and spermatogenesis, increased when animals were experimentally infected with Bd . In P. corroboree , infected males have thicker germinal epithelium, and a larger proportion of spermatocytes. In L. v. alpina , infected males had more spermatic cell bundles in total, and a larger proportion of spermatozoa bundles. In female L. v. alpina , ovaries and oviducts were larger in infected animals, and there were more cells present within the ovaries. Terminal investment has consequences for the evolution of disease resistance in declining species. If infected animals are increasing reproductive efforts and producing more offspring before succumbing to disease, it is possible that population-level selection for disease resistance will be minimized.

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Habitat fragmentation in the Brazilian Atlantic Forest is associated with erosion of frog immunogenetic diversity and increased fungal infections

10.22541/au.161054186.64043009/v1 ◽

2021 ◽

Author(s):

Anat Belasen ◽

Kevin Amses ◽

Rebecca Clemons ◽

Guilherme Becker ◽

Felipe Toledo ◽

...

Keyword(s):

Habitat Fragmentation ◽

Atlantic Forest ◽

Batrachochytrium Dendrobatidis ◽

Fungal Infections ◽

Emerging Infectious Diseases ◽

Genetic Erosion ◽

Population Level ◽

Brazilian Atlantic Forest ◽

Frog Species ◽

Mhc Iib

Habitat fragmentation and infectious disease threaten amphibians globally, but little is known about how these two threats interact. In this study, we examined the effects of Brazilian Atlantic Forest habitat fragmentation on frog genetic diversity at an immune locus known to affect disease susceptibility in amphibians, the MHC IIB locus. We used a custom high-throughput assay to sequence the MHC IIB locus across six focal frog species in two regions of the Atlantic Forest. We also used a molecular assay to quantify infections by the fungal pathogen Batrachochytrium dendrobatidis (Bd). We found that habitat fragmentation is associated with genetic erosion at the MHC IIB locus, and that this erosion is most severe in frog species restricted to intact forests. Significant Bd infections were recovered only in one Atlantic Forest region, potentially due to the relatively higher elevation. In this region, forest specialists showed an increase in both Bd prevalence and loads in fragmented habitats. We also found that reduced population-level MHC IIB diversity was associated with increased Bd infection risk. On the individual-level, MHC IIB heterozygotes (by allelic genotype as well as supertype) exhibited a reduced risk of Bd infection. Our results suggest that habitat fragmentation increases infection susceptibility in amphibians, mediated at least in part through loss of immunogenetic diversity. Our findings have implications for the conservation of fragmented populations in the face of emerging infectious diseases.

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Older conservatives: reproduction in female Alpine chamois (Rupicapra rupicapra) is increasingly risk-averse with age

Canadian Journal of Zoology ◽

10.1139/cjz-2015-0153 ◽

2016 ◽

Vol 94 (5) ◽

pp. 311-321 ◽

Cited By ~ 12

Author(s):

A. Morin ◽

M. Rughetti ◽

S. Rioux-Paquette ◽

M. Festa-Bianchet

Keyword(s):

Reproductive Success ◽

Reproductive Effort ◽

Risk Averse ◽

Costs Of Reproduction ◽

Rupicapra Rupicapra ◽

Terminal Investment ◽

Age Dependent ◽

Alpine Chamois ◽

Old Females ◽

Investment Hypothesis

In long-lived mammals, costs of reproduction may vary with age. The terminal investment hypothesis predicts greater reproductive effort as females approach the end of their life expectancy. We monitored 97 individually marked female Alpine chamois (Rupicapra rupicapra (L., 1758)) between 2007 and 2013 to determine how age-specific reproduction affected body mass and subsequent reproductive success. We captured and weighed females between April and August and monitored reproductive success from April to October through mother–kid associations. Reproductive success was strongly age-dependent and peaked at 70% for prime-aged females (4–7 years). Reproductive senescence began at 8 years, earlier than reported by other studies of ungulates. There was no clear evidence of reproductive costs in any age class. Reproductive success was very heterogeneous for old females, suggesting variability in the onset of senescence. Old females were less likely to reproduce in poor years despite being heavier than prime-aged females, suggesting reproductive restraint in late life rather than terminal investment. Female mass remained stable from May to August with no effect of lactation. Our results suggest that chamois reproductive strategy becomes increasingly conservative with age, resulting in no detectable costs of reproduction.

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Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2006.3480 ◽

2006 ◽

Vol 273 (1593) ◽

pp. 1443-1448 ◽

Cited By ~ 176

Author(s):

Alberto Velando ◽

Hugh Drummond ◽

Roxana Torres

Keyword(s):

Reproductive Success ◽

Reproductive Effort ◽

Initial Increase ◽

Male Reproductive Success ◽

Age Classes ◽

Theoretical Idea ◽

Sula Nebouxii ◽

Terminal Investment ◽

Survival And Reproduction ◽

Investment Hypothesis

This study reports an experimental confirmation of the terminal investment hypothesis, a longstanding theoretical idea that animals should increase their reproductive effort as they age and their prospects for survival and reproduction decline. Previous correlational and experimental attempts to test this hypothesis have yielded contradictory results. In the blue-footed booby, Sula nebouxii , a long-lived bird, after initial increase, male reproductive success declines progressively with age. Before laying, males of two age classes were challenged with lipopolysaccharide to elicit an immune response, which induced symptoms of declining survival prospects. Reproductive success of immune-challenged mature males fell, while that of immune-challenged old males showed a 98% increase. These results demonstrate that senescent males with poor reproductive prospects increase their effort when those prospects are threatened, whereas younger males with good reproductive prospects do not.

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Faculty Opinions recommendation of Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1032702.374472 ◽

2006 ◽

Author(s):

Gabriele Sorci

Keyword(s):

Reproductive Effort ◽

Terminal Investment ◽

Investment Hypothesis

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Genetic potential for disease resistance in a critically endangered frog decimated by chytridiomycosis

10.1101/247999 ◽

2018 ◽

Cited By ~ 1

Author(s):

Tiffany A. Kosch ◽

Catarina N. S. Silva ◽

Laura A. Brannelly ◽

Alexandra A. Roberts ◽

Quintin Lau ◽

...

Keyword(s):

Genetic Diversity ◽

Disease Resistance ◽

Batrachochytrium Dendrobatidis ◽

Population Level ◽

Nucleotide Polymorphisms ◽

High Genetic Diversity ◽

Southeastern Australia ◽

Challenge Study ◽

In The Wild ◽

Functional Extinction

AbstractSouthern corroboree frogs (Pseudophryne corroboree) have been driven to functional extinction in the wild after the emergence of the amphibian fungal pathogen Batrachochytrium dendrobatidis (Bd) in southeastern Australia in the 1980s. This species is currently maintained in a captive assurance colony and is managed to preserve the genetic diversity of the founding populations. However, it is unlikely that self-sustaining wild populations can be re-established unless Bd resistance increases. We performed a Bd-challenge study to investigate the association between genetic variants of the major histocompatibility complex class IA (MHC) and genome-wide single nucleotide polymorphisms (SNPs). We also investigated differences in Bd susceptibility among individuals and populations, and the genetic diversity and population genetic structure of four natural P. corroboree populations. We found several MHC alleles and SNPs associated with Bd infection load and survival, provide evidence of significant structure among populations, and identified population-level differences in the frequency of influential variants. We also detected evidence of positive selection acting on the MHC and a subset of SNPs as well as evidence of high genetic diversity in P. corroboree populations. We suggest that low interbreeding rates may have contributed to the demise of this species by limiting the spread of Bd resistance genes. However, our findings demonstrate that despite dramatic declines there is potential to restore high levels of genetic diversity in P. corroboree. Additionally, we show that there are immunogenetic differences among captive southern corroboree frogs, which could be manipulated to increase disease resistance and mitigate the key threatening process, chytridiomycosis.

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Ant queens increase their reproductive efforts after pathogen infection

Royal Society Open Science ◽

10.1098/rsos.170547 ◽

2017 ◽

Vol 4 (7) ◽

pp. 170547 ◽

Cited By ~ 14

Author(s):

Julia Giehr ◽

Anna V. Grasse ◽

Sylvia Cremer ◽

Jürgen Heinze ◽

Alexandra Schrempf

Keyword(s):

Social Insect ◽

Reproductive Effort ◽

Reproductive Rate ◽

Egg Laying ◽

Reproductive Value ◽

Reproductive Senescence ◽

Terminal Investment ◽

Investment In Reproduction ◽

First Time ◽

Investment Hypothesis

Infections with potentially lethal pathogens may negatively affect an individual's lifespan and decrease its reproductive value. The terminal investment hypothesis predicts that individuals faced with a reduced survival should invest more into reproduction instead of maintenance and growth. Several studies suggest that individuals are indeed able to estimate their body condition and to increase their reproductive effort with approaching death, while other studies gave ambiguous results. We investigate whether queens of a perennial social insect (ant) are able to boost their reproduction following infection with an obligate killing pathogen. Social insect queens are special with regard to reproduction and aging, as they outlive conspecific non-reproductive workers. Moreover, in the ant Cardiocondyla obscurior , fecundity increases with queen age. However, it remained unclear whether this reflects negative reproductive senescence or terminal investment in response to approaching death. Here, we test whether queens of C. obscurior react to infection with the entomopathogenic fungus Metarhizium brunneum by an increased egg-laying rate. We show that a fungal infection triggers a reinforced investment in reproduction in queens. This adjustment of the reproductive rate by ant queens is consistent with predictions of the terminal investment hypothesis and is reported for the first time in a social insect.

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Faculty Opinions recommendation of Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1013136.189206 ◽

2003 ◽

Author(s):

Thomas Mitchell-Olds

Keyword(s):

Arabidopsis Thaliana ◽

Disease Resistance ◽

Natural Selection ◽

Resistance Gene ◽

Disease Resistance Gene ◽

Selection For

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Developmental morphology and anatomy of the reproductive structures in sunflower (Helianthus annuus): a unified temporal scale

Botany ◽

10.1139/cjb-2014-0245 ◽

2015 ◽

Vol 93 (5) ◽

pp. 307-316 ◽

Cited By ~ 2

Author(s):

L.I. Lindström ◽

L.F. Hernández

Keyword(s):

Disease Resistance ◽

Helianthus Annuus ◽

Oil Content ◽

Genetic Selection ◽

Reproductive Development ◽

Developmental Morphology ◽

Male And Female ◽

Reproductive Structures ◽

Selection For ◽

Growing Conditions

In sunflower (Helianthus annuus L.), there has been an intense genetic selection for achenes with agronomic value, such as greater mass, oil content, and disease resistance. However, the information regarding the anatomical events that control their growth and maturation is surprisingly scarce. The aim of the present work was to study sunflower male and female sporogenesis and gametogenesis, as well as cell division and enlargement and tissue differentiation in the ovary and the embryo, linking the timing of these events to two frequently used phenological scales and a thermal time scale. In addition, we propose an ontogenetic scale that integrates the results of the present work to that of previous studies on sunflower reproductive development. The unified scales presented here provide a framework for others to investigate the relationships uncovered in this study in different genetic backgrounds and under different growing conditions.

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