Lectin staining and flow cytometry reveals female-induced sperm acrosome reaction and surface carbohydrate reorganization

Kekäläinen, Jukka; Larma, Irma; Linden, Matthew D.; Evans, Jonathan P.

doi:10.1038/srep15321

Cited by 20 publications

(33 citation statements)

References 58 publications

(80 reference statements)

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“…To date, only a few EC molecules have been identified in broadcast spawning species (e.g., Böhmer et al, ; Riffell, Krug, & Zimmer, ; Ward, Brokaw, Garbers, & Vacquier, ; Yoshida, Murata, Inaba, & Morisawa, ) and we currently have no information in this regard for M. galloprovincialis . Furthermore, it would be interesting to examine the effect of OA on EC‐induced changes in sperm physiology, for example, pH i changes and influx of calcium when mixed with ECs (e.g., see the techniques used in Kekäläinen & Evans, ; Kekäläinen, Larma, Linden, & Evans, ). Such studies would provide a detailed understanding of cellular and biochemical processes underlying the effects of OA on gamete interactions.…”

Section: Discussionmentioning

confidence: 99%

Ocean acidification during prefertilization chemical communication affects sperm success

Lymbery

Kennington

Cornwall

et al. 2019

Ecology and Evolution

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Ocean acidification (OA) poses a major threat to marine organisms, particularly during reproduction when externally shed gametes are vulnerable to changes in seawater pH. Accordingly, several studies on OA have focused on how changes in seawater pH influence sperm behavior and/or rates of in vitro fertilization. By contrast, few studies have examined how pH influences prefertilization gamete interactions, which are crucial during natural spawning events in most externally fertilizing taxa. One mechanism of gamete interaction that forms an important component of fertilization in most taxa is communication between sperm and egg‐derived chemicals. These chemical signals, along with the physiological responses in sperm they elicit, are likely to be highly sensitive to changes in seawater chemistry. In this study, we experimentally tested this possibility using the blue mussel, Mytilus galloprovincialis, a species in which females have been shown to use egg‐derived chemicals to promote the success of sperm from genetically compatible males. We conducted trials in which sperm were allowed to swim in gradients of egg‐derived chemicals under different seawater CO2 (and therefore pH) treatments. We found that sperm had elevated fertilization rates after swimming in the presence of egg‐derived chemicals in low pH (pH 7.6) compared with ambient (pH 8.0) seawater. This observed effect could have important implications for the reproductive fitness of external fertilizers, where gamete compatibility plays a critical role in modulating reproduction in many species. For example, elevated sperm fertilization rates might disrupt the eggs' capacity to avoid fertilizations by genetically incompatible sperm. Our findings highlight the need to understand how OA affects the multiple stages of sperm‐egg interactions and to develop approaches that disentangle the implications of OA for female, male, and population fitness.

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Section: Discussionmentioning

confidence: 99%

Ocean acidification during prefertilization chemical communication affects sperm success

Lymbery

Kennington

Cornwall

et al. 2019

Ecology and Evolution

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“…; Kekäläinen et al. ). These modifications and properties of sperm outer membranes are critical regulators of sperm motility and essential determinants of sperm capacitation, the acrosome reaction, and ultimately successful fertilization.…”

Section: Discussionmentioning

confidence: 99%

“…Each sperm sample was then stained with 10 μg/mL of FITC‐labeled WGA lectin (which has been demonstrated to be especially suitable marker for egg water‐induced change in sperm physiology: Kekäläinen et al. ) and 1 μM of FLUO‐4 calcium indicator (Molecular Probes Inc., Eugene, OR). To facilitate cell loading, FLUO‐4–labeled samples also contained 0.02% w/v of Pluronic ® F‐127 (Molecular Probes Inc.).…”

Section: Methodsmentioning

confidence: 99%

“…Based on the FSC and SSC the sperm population was then divided into two nonoverlapping subpopulations representing acrosome reacted and nonreacted sperm, respectively (see Kekäläinen et al. , for details). We determined mean values of FSC, SSC, and fluorescence intensity (for four lectins and FLUO‐4) for all three sperm populations (all sperm, acrosome‐reacted cells, and nonreacted cells) and also determined the percentage of acrosome‐reacted cells in each sample: (number of reacted cells/number of all sperm) × 100.…”

Section: Methodsmentioning

confidence: 99%

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Female-induced remote regulation of sperm physiology may provide opportunities for gamete-level mate choice

Kekäläinen

Evans

2016

Evolution

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In sedentary externally fertilizing species, direct interactions between mating partners are limited and prefertilization communication between sexes occurs largely at the gamete level. Certain combinations of eggs and sperm often have higher fertilization success than others, which may be contingent on egg-derived chemical factors that preferentially attract sperm from compatible males. Here, we examine the mechanisms underlying such effects in the marine mussel Mytilus galloprovincialis, where differential sperm attraction has recently been shown to be associated with variation in offspring viability. Specifically, we focus on the sperm surface glycans, an individually unique layer of carbohydrates that moderate self-recognition and other cellular-level interactions. In many species egg-derived factors trigger remarkable changes in the sperm's glycan layer, physiology, and swimming behavior, and thus potentially moderate mate choice at the gamete level. Here, we show that sperm glycan modifications and the strength of acrosome reaction are both dependent on specific male-female interactions (male-female combination). We also find associations between female-induced sperm glycan changes and the Ca influx into sperm--a key regulator of fertilization processes from sperm capacitation to gamete fusion. Together, our results suggest that female-induced remote regulation of sperm physiology may constitute a novel mechanism of gamete-level mate choice.

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“…We suspect that sperm chemotaxis, and similar chemically moderated processes that influence gamete behaviour (see § §3 and 5), may serve as moderators of mate choice at the gamete level, in both internally and externally fertilizing species. We eagerly await further insights from plants, fungi and broadcast spawners, some of which are already uncovering putative mechanisms of gamete choice moderated by female reproductive secretions [147]. In this way, we anticipate that that such studies will stimulate research on 'the usual organisms' to better understand the adaptive function of female reproductive secretion in these species.…”

Section: Discussionmentioning

confidence: 99%

Sexual selection in hermaphrodites, sperm and broadcast spawners, plants and fungi

Beekman

Nieuwenhuis

Ortiz‐Barrientos

et al. 2016

Phil. Trans. R. Soc. B

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One contribution of 15 to a theme issue 'Weird sex: the underappreciated diversity of sexual reproduction'. Darwin was the first to recognize that sexual selection is a strong evolutionary force. Exaggerated traits allow same-sex individuals to compete over access to mates and provide a mechanism by which mates are selected. It is relatively easy to appreciate how inter-and intrasexual selection work in organisms with the sensory capabilities to perceive physical or behavioural traits that signal mate quality or mate compatibility, and to assess the relative quality of competitors. It is therefore not surprising that most studies of sexual selection have focused on animals with separate sexes and obvious adaptations that function in the context of reproductive competition. Yet, many sexual organisms are both male and female at the same time, often lack sexual dimorphism and never come into direct contact at mating. How does sexual selection act in such species, and what can we learn from them? Here, we address these questions by exploring the potential for sexual selection in simultaneous hermaphrodites, sperm-and broadcast spawners, plants and fungi. Our review reveals a range of mechanisms of sexual selection, operating primarily after gametes have been released, which are common in many of these groups and also quite possibly in more familiar (internally fertilizing and sexually dimorphic) organisms.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.

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Lectin staining and flow cytometry reveals female-induced sperm acrosome reaction and surface carbohydrate reorganization

Cited by 20 publications

References 58 publications

Ocean acidification during prefertilization chemical communication affects sperm success

Ocean acidification during prefertilization chemical communication affects sperm success

Female-induced remote regulation of sperm physiology may provide opportunities for gamete-level mate choice

Sexual selection in hermaphrodites, sperm and broadcast spawners, plants and fungi

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