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Abstract Interactions between spermatozoa and the female reproductive tract (FRT) are complex, in many cases poorly understood, and likely to contribute to the mechanistic basis of idiopathic infertility. As such, it is not surprising that the FRT was often viewed historically as a “hostile” environment for spermatozoa. The FRT has also been touted as a selective environment to ensure that only the highest quality spermatozoa progress to the oocyte for the opportunity to participate in fertilization. Recent advances, however, are giving rise to a far more nuanced view in which supportive spermatozoa × FRT interactions—in both directions—contribute to beneficial, even essential, effects on fertility. In this perspective article, we discuss several examples of positive spermatozoa × FRT interactions. We believe that these examples, arising in part from studies of taxonomically diverse nonmammalian systems, are useful to efforts to study mammalian spermatozoa × FRT interactions and their relevance to fertility and the advancement of assisted reproductive technologies. 

Interactions between sperm and the female reproductive tract (FRT) are critical to reproductive success and yet are poorly understood. Because sperm complete their functional maturation within the FRT, the life history of sperm is likely to include a molecular “hand-off” from males to females. Although such intersexual molecular continuity is likely to be widespread among all internally fertilizing species, the identity and extent of female contributions are largely unknown. We combined semiquantitative proteomics with sex-specific isotopic labeling to catalog the posttesticular life history of the sperm proteome and determine the extent of molecular continuity between male and FRTs. We show that the Drosophila melanogaster sperm proteome undergoes substantial compositional changes after being transferred to the FRT. Multiple seminal fluid proteins initially associate with sperm, but most become undetectable after sperm are stored. Female-derived proteins also begin to associate with sperm immediately after mating, and they comprise nearly 20% of the postmating sperm proteome following 4 d of storage in the FRT. Female-derived proteins that associate with sperm are enriched for processes associated with energy metabolism, suggesting that female contributions support sperm viability during the prolonged period between copulation and fertilization. Our research provides a comprehensive characterization of sperm proteome dynamics and expands our understanding of the critical process of sperm–FRT interactions. 

The neprilysin (M13) family of metalloendopeptidases comprises highly conserved ectoenzymes that cleave and thereby inactivate many physiologically relevant peptides in the extracellular space. Impaired neprilysin activity is associated with numerous human diseases. Here, we present a comprehensive list and classification of M13 family members in Drosophila melanogaster. Seven Neprilysin (Nep) genes encode active peptidases, while 21 Neprilysin-like (Nepl) genes encode proteins predicted to be catalytically inactive. RNAseq data demonstrate that all 28 genes are expressed during development, often in a tissue-specific pattern. Most Nep proteins possess a transmembrane domain, whereas almost all Nepl proteins are predicted to be secreted. 

Drosophila melanogasterfemales experience a large shift in energy homeostasis after mating to compensate for nutrient investment in egg production. To cope with this change in metabolism, mated females undergo widespread physiological and behavioral changes, including increased food intake and altered digestive processes. The mechanisms by which the female digestive system responds to mating remain poorly characterized. Here, we demonstrate that the seminal fluid protein Sex Peptide (SP) is a key modulator of female post-mating midgut growth and gene expression. SP is both necessary and sufficient to trigger post-mating midgut growth in females under normal nutrient conditions, and likely acting via its receptor, Sex Peptide Receptor (SPR). Moreover, SP is responsible for almost the totality of midgut transcriptomic changes following mating, including up-regulation of protein and lipid metabolism genes and down-regulation of carbohydrate metabolism genes. These changes in metabolism may help supply the female with the nutrients required to sustain egg production. Thus, we report a role for SP in altering female physiology to enhance reproductive output: Namely, SP triggers the switch from virgin to mated midgut state.

 

Even in well-characterized genomes, many transcripts are considered noncoding RNAs (ncRNAs) simply due to the absence of large open reading frames (ORFs). However, it is now becoming clear that many small ORFs (smORFs) produce peptides with important biological functions. In the process of characterizing the ribosome-bound transcriptome of an important cell type of the seminal fluid-producing accessory gland of Drosophila melanogaster , we detected an RNA, previously thought to be noncoding, called male-specific abdominal ( msa ). Notably, msa is nested in the HOX gene cluster of the Bithorax complex and is known to contain a micro-RNA within one of its introns. We find that this RNA encodes a “micropeptide” (9 or 20 amino acids, MSAmiP) that is expressed exclusively in the secondary cells of the male accessory gland, where it seems to accumulate in nuclei. Importantly, loss of function of this micropeptide causes defects in sperm competition. In addition to bringing insights into the biology of a rare cell type, this work underlines the importance of small peptides, a class of molecules that is now emerging as important actors in complex biological processes. 

ABSTRACT We propose that insights from the field of evolutionary developmental biology (or ‘evo-devo’) provide a framework for an integrated understanding of the origins of behavioural diversity and its underlying mechanisms. Towards that goal, in this Commentary, we frame key questions in behavioural evolution in terms of molecular, cellular and network-level properties with a focus on the nervous system. In this way, we highlight how mechanistic properties central to evo-devo analyses – such as weak linkage, versatility, exploratory mechanisms, criticality, degeneracy, redundancy and modularity – affect neural circuit function and hence the range of behavioural variation that can be filtered by selection. We outline why comparative studies of molecular and neural systems throughout ontogeny will provide novel insights into diversity in neural circuits and behaviour. 

Synopsis Like many scientific disciplines, the field of reproductive biology is subject to biases in terminology and research foci. For example, females are often described as coy and passive players in reproductive behaviors and are termed “promiscuous” if they engage in extra-pair copulations. Males on the other hand are viewed as actively holding territories and fighting with other males. Males are termed “multiply mating” if they mate with multiple females. Similarly, textbooks often illustrate meiosis as it occurs in males but not females. This edition of Integrative and Comparative Biology (ICB) includes a series of papers that focus on reproduction from the female perspective. These papers represent a subset of the work presented in our symposium and complementary sessions on female reproductive biology. In this round table discussion, we use a question and answer format to leverage the diverse perspectives and voices involved with the symposium in an exploration of theoretical, cultural, pedagogical, and scientific issues related to the study of female biology. We hope this dialog will provide a stepping-stone toward moving reproductive science and teaching to a more inclusive and objective framework.