skip to main content


This content will become publicly available on September 1, 2024

Title: Reduced male fertility of an Antarctic mite following extreme heat stress could prompt localized population declines
Climate change is leading to substantial global thermal changes, which are particularly pronounced in polar regions. Few studies have examined the impact of heat stress on reproduction in Antarctic terrestrial arthropods, specifically how brief, extreme events may alter survival. We observed that sublethal heat stress reduces male fecundity in an Antarctic mite, yielding females that produced fewer viable eggs. Females and males collected from microhabitats with high temperatures showed a similar reduction in fertility. This impact is temporary, as indicated by recovery of male fecundity following return to cooler, stable conditions. The diminished fecundity is likely due to a drastic reduction in the expression of male-associated factors that occur in tandem with a substantial increase in the expression of heat shock proteins. Cross mating between mites from different sites confirmed that heat-exposed populations have impaired male fertility. However, the impact on fertility declines with time when the mites are allowed to recover under less stressful conditions, suggesting that the negative effects are transient. Modeling indicated that heat stress is likely to reduce population growth and that short bouts of non-lethal heat stress could have substantial effects on local populations of Antarctic arthropods.  more » « less
Award ID(s):
1654417
NSF-PAR ID:
10493068
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ;
Publisher / Repository:
Elsevier
Date Published:
Journal Name:
Cell Stress and Chaperones
Volume:
28
Issue:
5
ISSN:
1355-8145
Page Range / eLocation ID:
541 to 549
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Globally invasiveAedes aegyptidisseminate numerous arboviruses that impact human health. One promising method to controlAe. aegyptipopulations is transinfection withWolbachia pipientis, which naturally infects ~40–52% of insects but notAe. aegypti. Transinfection ofAe. aegyptiwith the wMelWolbachiastrain induces cytoplasmic incompatibility (CI), allows infected individuals to invade native populations, and inhibits transmission of medically relevant arboviruses by females. Female insects undergo post-mating physiological and behavioral changes—referred to as the female post-mating response (PMR)—required for optimal fertility. PMRs are typically elicited by male seminal fluid proteins (SFPs) transferred with sperm during mating but can be modified by other factors, including microbiome composition.Wolbachiahas modest effects onAe. aegyptifertility, but its influence on other PMRs is unknown. Here, we show thatWolbachiainfluences female fecundity, fertility, and re-mating incidence and significantly extends the longevity of virgin females. Using proteomic methods to examine the seminal proteome of infected males, we found thatWolbachiamoderately affects SFP composition. However, we identified 125 paternally transferredWolbachiaproteins, but the CI factor proteins (Cifs) were not among them. Our findings indicate thatWolbachiainfection ofAe. aegyptialters female PMRs, potentially influencing control programs that utilizeWolbachia-infected individuals.

     
    more » « less
  2. Abstract

    Polyphenism allows organisms to respond to varying environmental conditions by adopting alternative collections of morphological traits, often leading to different reproductive strategies. In many insects, polyphenism affecting the development of flight trades dispersal ability for increased fecundity. The soapberry bug Jadera haematoloma (Hemiptera: Rhopalidae) exhibits wing polyphenism in response to juvenile nutritional resources and cohort density. Development of full-length wings and flight-capable thoracic muscles occurs more frequently in cohorts raised under low food density conditions, and these features are correlated to reduced female fecundity. Soapberry bugs represent an example of polyphenic dispersal-fecundity trade-off. Short-wing development is not sex-limited, and morphs can also differ in male fertility. We have previously shown, via a candidate gene approach, that manipulation of insulin signaling can alter the threshold for nutritional response and that changes in the activity of this pathway underlie, at least in part, differences in the polyphenic thresholds in different host-adapted populations of J. haematoloma. We now expand the examination of this system using transcriptome sequencing across a multidimensional matrix of life stage, tissue, sex, food density, and host population. We also examine the use of wing and thorax shape as factors modeling gene expression. In addition to insulin signaling, we find that components of the TOR, Hippo, Toll, and estrogen-related receptor pathways are differentially expressed in the thorax of polyphenic morphs. The transcription factor Sox14 was one of the few genes differentially expressed in the gonads of morphs, being up-regulated in ovaries. We identify two transcription factors as potential mediators of morph-specific male fertility differences. We also find that bugs respond to nutrient limitation with expression of genes linked to cuticle structure and spermatogenesis. These findings provide a broad perspective from which to view this nutrition-dependent polyphenism.

     
    more » « less
  3. null (Ed.)
    Understanding the pleiotropic consequences of gene drive systems on host fitness is essential to predict their spread through a host population. Here, we study sex-ratio (SR) X-chromosome drive in the fly Drosophila recens , where SR causes the death of Y-bearing sperm in male carriers. SR males only sire daughters, which all carry SR, thus giving the chromosome a transmission advantage. The prevalence of the SR chromosome appears stable, suggesting pleiotropic costs. It was previously shown that females homozygous for SR are sterile, and here, we test for additional fitness costs of SR. We found that females heterozygous for SR have reduced fecundity and that male SR carriers have reduced fertility in conditions of sperm competition. We then use our fitness estimates to parametrize theoretical models of SR drive and show that the decrease in fecundity and sperm competition performance can account for the observed prevalence of SR in natural populations. In addition, we found that the expected equilibrium frequency of the SR chromosome is particularly sensitive to the degree of multiple mating and performance in sperm competition. Together, our data suggest that the mating system of the organism should be carefully considered during the development of gene drive systems. 
    more » « less
  4. Background Animal conservation often requires intensive management actions to improve reproductive output, yet any adverse effects of these may not be immediately apparent, particularly in threatened species with small populations and long lifespans. Hand-rearing is an example of a conservation management strategy which, while boosting populations, can cause long-term demographic and behavioural problems. It is used in the recovery of the critically endangered kākāpō ( Strigops habroptilus ), a flightless parrot endemic to New Zealand, to improve the slow population growth that is due to infrequent breeding, low fertility and low hatching success. Methods We applied Bayesian mixed models to examine whether hand-rearing and other factors were associated with clutch fertility in kākāpō. We used projection predictive variable selection to compare the relative contributions to fertility from the parents’ rearing environment, their age and previous copulation experience, the parental kinship, and the number of mates and copulations for each clutch. We also explored how the incidence of repeated copulations and multiple mates varied with kākāpō density. Results The rearing status of the clutch father and the number of mates and copulations of the clutch mother were the dominant factors in predicting fertility. Clutches were less likely to be fertile if the father was hand-reared compared to wild-reared, but there was no similar effect for mothers. Clutches produced by females copulating with different males were more likely to be fertile than those from repeated copulations with one male, which in turn had a higher probability of fertility than those from a single copulation. The likelihood of multiple copulations and mates increased with female:male adult sex ratio, perhaps as a result of mate guarding by females. Parental kinship, copulation experience and age all had negligible associations with clutch fertility. Conclusions These results provide a rare assessment of factors affecting fertility in a wild threatened bird species, with implications for conservation management. The increased fertility due to multiple mates and copulations, combined with the evidence for mate guarding and previous results of kākāpō sperm morphology, suggests that an evolutionary mechanism exists to optimise fertility through sperm competition in kākāpō. The high frequency of clutches produced from single copulations in the contemporary population may therefore represent an unnatural state, perhaps due to too few females. This suggests that opportunity for sperm competition should be maximised by increasing population densities, optimising sex ratios, and using artificial insemination. The lower fertility of hand-reared males may result from behavioural defects due to lack of exposure to conspecifics at critical development stages, as seen in other taxa. This potential negative impact of hand-rearing must be balanced against the short-term benefits it provides. 
    more » « less
  5. null (Ed.)
    Abstract The Antarctic midge, Belgica antarctica , is a wingless, non-biting midge endemic to Antarctica. Larval development requires at least 2 years, but adults live only 2 weeks. The nonfeeding adults mate in swarms and females die shortly after oviposition. Eggs are suspended in a gel of unknown composition that is expressed from the female accessory gland. This project characterizes molecular mechanisms underlying reproduction in this midge by examining differential gene expression in whole males, females, and larvae, as well as in male and female accessory glands. Functional studies were used to assess the role of the gel encasing the eggs, as well as the impact of stress on reproductive biology. RNA-seq analyses revealed sex- and development-specific gene sets along with those associated with the accessory glands. Proteomic analyses were used to define the composition of the egg-containing gel, which is generated during multiple developmental stages and derived from both the accessory gland and other female organs. Functional studies indicate the gel provides a larval food source as well as a buffer for thermal and dehydration stress. All of these function are critical to juvenile survival. Larval dehydration stress directly reduces production of storage proteins and key accessory gland components, a feature that impacts adult reproductive success. Modeling reveals that bouts of dehydration may have a significant impact on population growth. This work lays a foundation for further examination of reproduction in midges and provides new information related to general reproduction in dipterans. A key aspect of this work is that reproduction and stress dynamics, currently understudied in polar organisms, are likely to prove critical in determining how climate change will alter their survivability. 
    more » « less