Sperm Cyst "Looping": A Developmental Novelty Enabling Extreme Male Ornament Evolution.

Zeeshan A Syed,Stephanie Nguyen,Steve Dorus,Julie A Brill,Negar Nasirzadeh,Matthew M Hansen,Sarah Rice,Ethan M Leef,Siyuan Cong,Amaar Asif,Patrick M O’Grady,Scott Pitnick,Romano Dallai

doi:10.3390/cells10102762

Zeeshan A Syed, Stephanie Nguyen + Show 11 more

Open Access

https://doi.org/10.3390/cells10102762

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Abstract

Postcopulatory sexual selection is credited as a principal force behind the rapid evolution of reproductive characters, often generating a pattern of correlated evolution between interacting, sex-specific traits. Because the female reproductive tract is the selective environment for sperm, one taxonomically widespread example of this pattern is the co-diversification of sperm length and female sperm-storage organ dimension. In Drosophila, having testes that are longer than the sperm they manufacture was believed to be a universal physiological constraint. Further, the energetic and time costs of developing long testes have been credited with underlying the steep evolutionary allometry of sperm length and constraining sperm length evolution in Drosophila. Here, we report on the discovery of a novel spermatogenic mechanism—sperm cyst looping—that enables males to produce relatively long sperm in short testis. This phenomenon (restricted to members of the saltans and willistoni species groups) begins early during spermatogenesis and is potentially attributable to heterochronic evolution, resulting in growth asynchrony between spermatid tails and the surrounding spermatid and somatic cyst cell membranes. By removing the allometric constraint on sperm length, this evolutionary innovation appears to have enabled males to evolve extremely long sperm for their body mass while evading delays in reproductive maturation time. On the other hand, sperm cyst looping was found to exact a cost by requiring greater total energetic investment in testes and a pronounced reduction in male lifespan. We speculate on the ecological selection pressures underlying the evolutionary origin and maintenance of this unique adaptation.

Highlights

We further explore the adaptive value of cyst looping and its relationship to sperm length evolution by quantifying and comparing patterns of divergence in numerous other reproductive traits (i.e., seminal receptacle (SR) length, testis length, relative testis mass, number of sperm transferred per copulation, and female remating interval) and life-history traits within a phylogenetic analytical framework
Using light microscopy to examine cysts dissected intact from testes, complete looping was observed in all seven assessed members of the willistoni species group, whereas partial looping was observed in all five assessed members of the saltans species group
Transmission electron microscopy of the testes of D. willistoni and D. saltans confirmed the occurrence of cyst looping in situ for both species (Figure 2)

Summary

Introduction

Postcopulatory sexual selection theory, which includes the combinatorial selective effects of sperm competition [3] and cryptic female choice [4], and sexual conflict theory [5] have proven critical for understanding the origin and evolutionary maintenance of anisogamy [6,7,8], as well as the extraordinary diversification of gametes and other reproductive characters [9,10,11,12,13,14]. Our understanding of the precise role of sexual selection in driving the evolution of sperm form and function is still incomplete [15], the selective role of the female reproductive tract, in the case of internally fertilizing species, is clear. Morphological co-diversification of sperm length and some critical dimension(s) of the female reproductive tract (e.g., sperm-storage organ size or duct length) is one of the most taxonomically widespread patterns in the field of comparative reproductive biology [12,17]

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