Abstract
Mammals exhibit a tremendous amount of variation in sperm morphology and despite the acknowledgement of sperm structural diversity across taxa, its functional significance remains poorly understood. Of particular interest is the sperm of rodents. While most Eutherian mammal spermatozoa are relatively simple cells with round or paddle-shaped heads, rodent sperm are often more complex and, in many species, display a striking apical hook. The function of the sperm hook remains largely unknown, but it has been hypothesized to have evolved as an adaptation to inter-male sperm competition and thus has been implicated in increased swimming efficiency or in the formation of collective sperm movements. Here we empirically test these hypotheses within a single lineage of Peromyscus rodents, in which closely related species naturally vary in their mating systems, sperm head shapes, and propensity to form sperm aggregates of varying sizes. We performed sperm morphological analyses as well as in vitro analyses of sperm aggregation and motility to examine whether the sperm hook (i) morphologically varies across these species and (ii) associates with sperm competition, aggregation, or motility. We demonstrate inter-specific variation in the sperm hook and then show that hook width negatively associates with sperm aggregation and sperm swimming speed, signifying that larger hooks may be a hindrance to sperm movement within this group of mice. Finally, we confirmed that the sperm hook hinders motility within a subset of Peromyscus leucopus mice that spontaneously produced sperm with no or highly abnormal hooks. Taken together, our findings suggest that any adaptive value of the sperm hook is likely associated with a function other than inter-male sperm competition, such as interaction with ova or cumulous cells during fertilization, or migration through the complex female reproductive tract.
Highlights
The sperm cell has undergone dramatic evolutionary diversification and extreme modifications such as loss of the flagella, gigantism, polymorphism, or even adhesion with other sperm to form conjugates, as reviewed in [1,2]
Within the six focal species of Peromyscus mice used in this study, we found the hook is an allometric feature of the sperm head that significantly associates with other sperm head features; cells with longer and wider hooks or with a larger hook surface area tended to have longer (LM: F1,135 = 108.5, p < 0.001) and wider (LM: F1,135 = 104.9, p < 0.001)
Controlling for head length, apical hook length significantly differed across species (Table 2, Figure 2A), and pairwise comparisons adjusted for multiple comparisons using LSmeans revealed that P. eremicus produce the longest relative apical hooks (P < 0.05 for all pairwise comparisons), whereas P. maniculatus, P. leucopus, and P. californicus produce the shortest relative apical hooks (p > 0.05 for these pairwise comparisons)
Summary
The sperm cell has undergone dramatic evolutionary diversification and extreme modifications such as loss of the flagella, gigantism, polymorphism, or even adhesion with other sperm to form conjugates, as reviewed in [1,2]. A few rare species lack sperm hooks entirely [3,4,6,7,8], whereas some possess multiple sperm hooks [8,9,10,11]. Given that sperm cells shed most of their organelles and cytoplasm during development [13], the structures retained, including morphological head features such as the apical hook, are likely to confer an adaptive function [1], and references therein. Despite the attention this unique head structure has received over the last two decades, its functional significance remains poorly understood
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