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Spatial and temporal complexities of reproductive behavior and sex ratios: a case from parasitic insects.

Dittmar K, Morse S, Gruwell M, Mayberry J, DiBlasi E - PLoS ONE (2011)

Bottom Line: At emergence these parasites exhibit a significant and seasonally stable female biased sex ratio.Host capture experiments throughout the day show a statistically significant, but temporary male excess in bat flies on foraging bats.Our results highlight the importance of detailed natural history observations, and emphasize that ignoring the spatial and temporal heterogeneity of reproduction in any organism will lead to significant empirical sampling errors of sex ratios, and may obscure operational sex ratios.

View Article: PubMed Central - PubMed

Affiliation: State University of New York at Buffalo, Department of Biological Sciences and Graduate Program of Ecology, Evolution and Behavior, Buffalo, New York, United States of America. katharinad@gmail.com

ABSTRACT

Background: Sex ratios are important empirical data in predicting sex allocation strategy and selection in populations. Therefore, they should be sampled at crucial developmental steps before and after parental investment. In parasites with free-living (off-host) developmental stages the timing and method of sampling is not trivial, because ecological niches are frequently poorly known. Consequently, information is scarce for sex ratios of these parasites between conception and sexual maturity. Often, only data from adult parasites are available, which usually were collected from the parasite's hosts. Generally, these ratios are assumed to represent operational sex ratios.

Methodology/principal findings: We here report three years of empirical data on population sex differentials from a bat ectoparasite (Trichobius frequens) with off-host developmental stages. At emergence these parasites exhibit a significant and seasonally stable female biased sex ratio. This bias is lost in the adult population on the roosting host, which shows sex ratios at equality. This is best explained by a behaviorally driven, sex-dependent mortality differential. Because consistently only subsets of females are available to mate, the operational sex ratio in the population is likely male biased. Host capture experiments throughout the day show a statistically significant, but temporary male excess in bat flies on foraging bats. This phenomenon is partly driven by the diurnal rhythms of female larviposition, and partly due to parasites remaining in the bat roost during foraging. Because most previous research in bat flies is based only on foraging bats, female contributions to physical sex ratios have been underestimated.

Conclusion/significance: Our results highlight the importance of detailed natural history observations, and emphasize that ignoring the spatial and temporal heterogeneity of reproduction in any organism will lead to significant empirical sampling errors of sex ratios, and may obscure operational sex ratios.

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Schematic diagram comparing parasite demography on-host (right panel), and off-host (left panel).On-host a physical ratio of 1∶1 is observed. Red rectangle represents females with developing offspring, which are not available for reproduction. Females within green rectangle are a mixture of returning females, and teneral females (N). The green rectangles (male and female) on-host represent the operational sex ratio (OSR), which is likely male biased. Off-host, depositing females leave the hosts (1), and arrive at the pupal field (2), where they give birth to their offspring. Some die due to predation (skull), while new females and males emerge leave the field (3) and return to the general host population (4). Mating ensues, and females become unavailable for mating. The ratio of males and females at emergence is skewed towards females.
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pone-0019438-g006: Schematic diagram comparing parasite demography on-host (right panel), and off-host (left panel).On-host a physical ratio of 1∶1 is observed. Red rectangle represents females with developing offspring, which are not available for reproduction. Females within green rectangle are a mixture of returning females, and teneral females (N). The green rectangles (male and female) on-host represent the operational sex ratio (OSR), which is likely male biased. Off-host, depositing females leave the hosts (1), and arrive at the pupal field (2), where they give birth to their offspring. Some die due to predation (skull), while new females and males emerge leave the field (3) and return to the general host population (4). Mating ensues, and females become unavailable for mating. The ratio of males and females at emergence is skewed towards females.

Mentions: Previous studies asserted that males prefer virgin females (tenerals) as mates [8]. Because the bulk of mating activity is reported to occur on roosting bats, it is likely that the operational sex ratio is in fact male biased (Table 1, Figure 6). The rationale for this assertion lies in the fact that although the physical sex ratio on roosting bats is at equilibrium, females with developing offspring will be unavailable for mating, because each new offspring requires a separate insemination event, and males are not attracted to “pregnant” females [8]. Thus it is likely, that all males compete for a subset of available females, which is mainly composed of teneral females (Figure 6). This scenario also predicts that males are the predominant competitors in this system, have a lower parental investment, as well as a higher potential to mate [4]. Given that reproductive behavior seems to be very similar across bat fly species, a male biased OSR may be a more general trend in bat flies than previously assumed.


Spatial and temporal complexities of reproductive behavior and sex ratios: a case from parasitic insects.

Dittmar K, Morse S, Gruwell M, Mayberry J, DiBlasi E - PLoS ONE (2011)

Schematic diagram comparing parasite demography on-host (right panel), and off-host (left panel).On-host a physical ratio of 1∶1 is observed. Red rectangle represents females with developing offspring, which are not available for reproduction. Females within green rectangle are a mixture of returning females, and teneral females (N). The green rectangles (male and female) on-host represent the operational sex ratio (OSR), which is likely male biased. Off-host, depositing females leave the hosts (1), and arrive at the pupal field (2), where they give birth to their offspring. Some die due to predation (skull), while new females and males emerge leave the field (3) and return to the general host population (4). Mating ensues, and females become unavailable for mating. The ratio of males and females at emergence is skewed towards females.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3091855&req=5

pone-0019438-g006: Schematic diagram comparing parasite demography on-host (right panel), and off-host (left panel).On-host a physical ratio of 1∶1 is observed. Red rectangle represents females with developing offspring, which are not available for reproduction. Females within green rectangle are a mixture of returning females, and teneral females (N). The green rectangles (male and female) on-host represent the operational sex ratio (OSR), which is likely male biased. Off-host, depositing females leave the hosts (1), and arrive at the pupal field (2), where they give birth to their offspring. Some die due to predation (skull), while new females and males emerge leave the field (3) and return to the general host population (4). Mating ensues, and females become unavailable for mating. The ratio of males and females at emergence is skewed towards females.
Mentions: Previous studies asserted that males prefer virgin females (tenerals) as mates [8]. Because the bulk of mating activity is reported to occur on roosting bats, it is likely that the operational sex ratio is in fact male biased (Table 1, Figure 6). The rationale for this assertion lies in the fact that although the physical sex ratio on roosting bats is at equilibrium, females with developing offspring will be unavailable for mating, because each new offspring requires a separate insemination event, and males are not attracted to “pregnant” females [8]. Thus it is likely, that all males compete for a subset of available females, which is mainly composed of teneral females (Figure 6). This scenario also predicts that males are the predominant competitors in this system, have a lower parental investment, as well as a higher potential to mate [4]. Given that reproductive behavior seems to be very similar across bat fly species, a male biased OSR may be a more general trend in bat flies than previously assumed.

Bottom Line: At emergence these parasites exhibit a significant and seasonally stable female biased sex ratio.Host capture experiments throughout the day show a statistically significant, but temporary male excess in bat flies on foraging bats.Our results highlight the importance of detailed natural history observations, and emphasize that ignoring the spatial and temporal heterogeneity of reproduction in any organism will lead to significant empirical sampling errors of sex ratios, and may obscure operational sex ratios.

View Article: PubMed Central - PubMed

Affiliation: State University of New York at Buffalo, Department of Biological Sciences and Graduate Program of Ecology, Evolution and Behavior, Buffalo, New York, United States of America. katharinad@gmail.com

ABSTRACT

Background: Sex ratios are important empirical data in predicting sex allocation strategy and selection in populations. Therefore, they should be sampled at crucial developmental steps before and after parental investment. In parasites with free-living (off-host) developmental stages the timing and method of sampling is not trivial, because ecological niches are frequently poorly known. Consequently, information is scarce for sex ratios of these parasites between conception and sexual maturity. Often, only data from adult parasites are available, which usually were collected from the parasite's hosts. Generally, these ratios are assumed to represent operational sex ratios.

Methodology/principal findings: We here report three years of empirical data on population sex differentials from a bat ectoparasite (Trichobius frequens) with off-host developmental stages. At emergence these parasites exhibit a significant and seasonally stable female biased sex ratio. This bias is lost in the adult population on the roosting host, which shows sex ratios at equality. This is best explained by a behaviorally driven, sex-dependent mortality differential. Because consistently only subsets of females are available to mate, the operational sex ratio in the population is likely male biased. Host capture experiments throughout the day show a statistically significant, but temporary male excess in bat flies on foraging bats. This phenomenon is partly driven by the diurnal rhythms of female larviposition, and partly due to parasites remaining in the bat roost during foraging. Because most previous research in bat flies is based only on foraging bats, female contributions to physical sex ratios have been underestimated.

Conclusion/significance: Our results highlight the importance of detailed natural history observations, and emphasize that ignoring the spatial and temporal heterogeneity of reproduction in any organism will lead to significant empirical sampling errors of sex ratios, and may obscure operational sex ratios.

Show MeSH