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Polyandry in the medfly - shifts in paternity mediated by sperm stratification and mixing.

Scolari F, Yuval B, Gomulski LM, Schetelig MF, Gabrieli P, Bassetti F, Wimmer EA, Malacrida AR, Gasperi G - BMC Genet. (2014)

Bottom Line: In the Mediterranean fruit fly (medfly), Ceratitis capitata, a highly invasive agricultural pest species, polyandry, associated with sperm precedence, is a recurrent behaviour in the wild.The accumulation of sperm from different males will increase the overall genetic variability of the offspring and will ultimately affect the effective population size.Indeed, even if the female's last mate is sterile, an increasing proportion of sperm from a previous mating with a fertile male may contribute to sire viable progeny.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: In the Mediterranean fruit fly (medfly), Ceratitis capitata, a highly invasive agricultural pest species, polyandry, associated with sperm precedence, is a recurrent behaviour in the wild. The absence of tools for the unambiguous discrimination between competing sperm from different males in the complex female reproductive tract has strongly limited the understanding of mechanisms controlling sperm dynamics and use.

Results: Here we use transgenic medfly lines expressing green or red fluorescent proteins in the spermatozoa, which can be easily observed and unambiguously differentiated within the female fertilization chamber. In twice-mated females, one day after the second mating, sperm from the first male appeared to be homogenously distributed all over the distal portion of each alveolus within the fertilization chamber, whereas sperm from the second male were clearly concentrated in the central portion of each alveolus. This distinct stratified sperm distribution was not maintained over time, as green and red sperm appeared homogeneously mixed seven days after the second mating. This dynamic sperm storage pattern is mirrored by the paternal contribution in the progeny of twice-mated females.

Conclusions: Polyandrous medfly females, unlike Drosophila, conserve sperm from two different mates to fertilize their eggs. From an evolutionary point of view, the storage of sperm in a stratified pattern by medfly females may initially favour the fresher ejaculate from the second male. However, as the second male's sperm gradually becomes depleted, the sperm from the first male becomes increasingly available for fertilization. The accumulation of sperm from different males will increase the overall genetic variability of the offspring and will ultimately affect the effective population size. From an applicative point of view, the dynamics of sperm storage and their temporal use by a polyandrous female may have an impact on the Sterile Insect Technique (SIT). Indeed, even if the female's last mate is sterile, an increasing proportion of sperm from a previous mating with a fertile male may contribute to sire viable progeny.

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Confocal merged images of fertilization chambers of twice-mated females. Green sperm was transferred by the first male (tGFP1 line) and the red sperm (DsRedEx1 line) by the second male. In 3A, the fertilization chamber was dissected 24h after the remating and immediately observed. In 3B, the fertilization chamber was dissected seven days after the remating. The two squares at the bottom of each picture show, from the left, the single red and green unmerged images, respectively. Scale bar = 15 µm.
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Figure 3: Confocal merged images of fertilization chambers of twice-mated females. Green sperm was transferred by the first male (tGFP1 line) and the red sperm (DsRedEx1 line) by the second male. In 3A, the fertilization chamber was dissected 24h after the remating and immediately observed. In 3B, the fertilization chamber was dissected seven days after the remating. The two squares at the bottom of each picture show, from the left, the single red and green unmerged images, respectively. Scale bar = 15 µm.

Mentions: We used both an epifluorescence and a confocal microscope-based approach to visualize the dynamics of the transgenic green and red sperm within the fertilization chamber of either once- and twice-mated wild-type females. In the fertilization chamber of once-mated females, either tGFP1 or DsRedEx1 sperm appeared to be clearly distributed in all the alveoli, where numerous bundles of coiled spermatozoa were visible (Figure 2). In the fertilization chambers of twice-mated females 24 h after the second copulation, the sperm from the first male appeared to be homogenously distributed all over the distal portion of each alveolus, whereas sperm from the second male were clearly concentrated in the central portion of each alveolus (Figure 3A). This distribution was evident in both the reciprocal parental male combinations. Seven days after remating, this distinct stratified sperm distribution was no longer evident. The green and the red sperm were homogeneously mixed, occupying the complete cavity of each alveolus (Figure 3B).


Polyandry in the medfly - shifts in paternity mediated by sperm stratification and mixing.

Scolari F, Yuval B, Gomulski LM, Schetelig MF, Gabrieli P, Bassetti F, Wimmer EA, Malacrida AR, Gasperi G - BMC Genet. (2014)

Confocal merged images of fertilization chambers of twice-mated females. Green sperm was transferred by the first male (tGFP1 line) and the red sperm (DsRedEx1 line) by the second male. In 3A, the fertilization chamber was dissected 24h after the remating and immediately observed. In 3B, the fertilization chamber was dissected seven days after the remating. The two squares at the bottom of each picture show, from the left, the single red and green unmerged images, respectively. Scale bar = 15 µm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4255777&req=5

Figure 3: Confocal merged images of fertilization chambers of twice-mated females. Green sperm was transferred by the first male (tGFP1 line) and the red sperm (DsRedEx1 line) by the second male. In 3A, the fertilization chamber was dissected 24h after the remating and immediately observed. In 3B, the fertilization chamber was dissected seven days after the remating. The two squares at the bottom of each picture show, from the left, the single red and green unmerged images, respectively. Scale bar = 15 µm.
Mentions: We used both an epifluorescence and a confocal microscope-based approach to visualize the dynamics of the transgenic green and red sperm within the fertilization chamber of either once- and twice-mated wild-type females. In the fertilization chamber of once-mated females, either tGFP1 or DsRedEx1 sperm appeared to be clearly distributed in all the alveoli, where numerous bundles of coiled spermatozoa were visible (Figure 2). In the fertilization chambers of twice-mated females 24 h after the second copulation, the sperm from the first male appeared to be homogenously distributed all over the distal portion of each alveolus, whereas sperm from the second male were clearly concentrated in the central portion of each alveolus (Figure 3A). This distribution was evident in both the reciprocal parental male combinations. Seven days after remating, this distinct stratified sperm distribution was no longer evident. The green and the red sperm were homogeneously mixed, occupying the complete cavity of each alveolus (Figure 3B).

Bottom Line: In the Mediterranean fruit fly (medfly), Ceratitis capitata, a highly invasive agricultural pest species, polyandry, associated with sperm precedence, is a recurrent behaviour in the wild.The accumulation of sperm from different males will increase the overall genetic variability of the offspring and will ultimately affect the effective population size.Indeed, even if the female's last mate is sterile, an increasing proportion of sperm from a previous mating with a fertile male may contribute to sire viable progeny.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: In the Mediterranean fruit fly (medfly), Ceratitis capitata, a highly invasive agricultural pest species, polyandry, associated with sperm precedence, is a recurrent behaviour in the wild. The absence of tools for the unambiguous discrimination between competing sperm from different males in the complex female reproductive tract has strongly limited the understanding of mechanisms controlling sperm dynamics and use.

Results: Here we use transgenic medfly lines expressing green or red fluorescent proteins in the spermatozoa, which can be easily observed and unambiguously differentiated within the female fertilization chamber. In twice-mated females, one day after the second mating, sperm from the first male appeared to be homogenously distributed all over the distal portion of each alveolus within the fertilization chamber, whereas sperm from the second male were clearly concentrated in the central portion of each alveolus. This distinct stratified sperm distribution was not maintained over time, as green and red sperm appeared homogeneously mixed seven days after the second mating. This dynamic sperm storage pattern is mirrored by the paternal contribution in the progeny of twice-mated females.

Conclusions: Polyandrous medfly females, unlike Drosophila, conserve sperm from two different mates to fertilize their eggs. From an evolutionary point of view, the storage of sperm in a stratified pattern by medfly females may initially favour the fresher ejaculate from the second male. However, as the second male's sperm gradually becomes depleted, the sperm from the first male becomes increasingly available for fertilization. The accumulation of sperm from different males will increase the overall genetic variability of the offspring and will ultimately affect the effective population size. From an applicative point of view, the dynamics of sperm storage and their temporal use by a polyandrous female may have an impact on the Sterile Insect Technique (SIT). Indeed, even if the female's last mate is sterile, an increasing proportion of sperm from a previous mating with a fertile male may contribute to sire viable progeny.

Show MeSH
Related in: MedlinePlus