Rapid evolution by sexual selection in a wild, invasive mammal

Evolution ◽  
2020 ◽  
Vol 74 (4) ◽  
pp. 740-748
Author(s):  
M. Aaron Owen ◽  
David C. Lahti

Zootaxa ◽  
2021 ◽  
Vol 5061 (3) ◽  
pp. 523-544
Author(s):  
BRUNA EMILIA ROMAN ◽  
LILIAN MADI-RAVAZZI

Male terminalia in insects with internal fertilization evolve more rapidly than other structures. The aedeagus is the most variable structure, making it a valuable diagnostic feature to distinguish species. The saltans group Sturtevant of Drosophila Fallén contains sibling species, that can be distinguished by their aedeagi. Here, we revised and illustrated the morphology of the male terminalia of the following species: Drosophila prosaltans Duda, 1927; D. saltans Sturtevant, 1916; D. lusaltans Magalhães, 1962; D. austrosaltans Spassky, 1957; D. septentriosaltans Magalhães, 1962; D. nigrosaltans Magalhães, 1962; D. pseudosaltans Magalhães, 1956; D. sturtevanti Duda, 1927; D. lehrmanae Madi-Ravazzi et al., 2021; D. dacunhai Mourão & Bicudo, 1967; D. milleri Magalhães, 1962; D. parasaltans Magalhães, 1956; D. emarginata Sturtevant, 1942; D. neoelliptica Pavan & Magalhães in Pavan, 1950; D. neosaltans Pavan & Magalhães in Pavan, 1950 and D. neocordata Magalhães, 1956. We found that phallic structures (e.g., the aedeagus) evolve more rapidly than periphallic structures (e.g., epandrium), being completely different among the subgroups and within them. This rapid evolution may be due to the action of sexual selection or to the potential role of those structures in speciation.  



2018 ◽  
Author(s):  
Joanna F. D. Hagen ◽  
Cláudia C. Mendes ◽  
Amber Blogg ◽  
Alex Payne ◽  
Kentaro M. Tanaka ◽  
...  

AbstractMale genital structures are among the most rapidly evolving morphological traits and are often the only features that can distinguish closely related species. This process is thought to be driven by sexual selection and may reinforce species separation. However, while the genetic basis of many phenotypic differences have been identified, we still lack knowledge about the genes underlying evolutionary differences in male genital organs and organ size more generally. The claspers (surstyli) are periphallic structures that play an important role in copulation in insects. Here we show that natural variation in clasper size and bristle number between Drosophila mauritiana and D. simulans is caused by evolutionary changes in tartan (trn), which encodes a transmembrane leucine-rich repeat domain protein that mediates cell-cell interactions and affinity differences. There are no fixed amino acid differences in trn between D. mauritiana and D. simulans but differences in the expression of this gene in developing genitalia suggest cis-regulatory changes in trn underlie the evolution of clasper morphology in these species. Finally, analysis of reciprocal hemizyotes that are genetically identical, except for which species the functional allele of trn is from, determined that the trn allele of D. mauritiana specifies larger claspers with more bristles than the allele of D. simulans. Therefore we have identified the first gene underlying evolutionary change in the size of a male genital organ, which will help to better understand the rapid diversification of these structures and the regulation and evolution of organ size more broadly.Significance StatementThe morphology of male genital organs evolves rapidly driven by sexual selection. However, little is known about the genes underlying genitalia differences between species. Identifying these genes is key to understanding how sexual selection acts on development to produce rapid phenotypic change. We have found that the gene tartan underlies differences between male Drosophila mauritiana and D. simulans in the size and bristle number of the claspers - genital projections that grasp the female during copulation. Moreover, since tartan encodes a protein that is involved in cell affinity, this may represent a new developmental mechanism for morphological change. Therefore, our study provides new insights into genetic and developmental bases for the rapid evolution of male genitalia and organ size more generally.





eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Damien Beau Wilburn ◽  
Lisa M Tuttle ◽  
Rachel E Klevit ◽  
Willie J Swanson

Sexual selection can explain the rapid evolution of fertilization proteins, yet sperm proteins evolve rapidly even if not directly involved in fertilization. In the marine mollusk abalone, sperm secrete enormous quantities of two rapidly evolving proteins, lysin and sp18, that are stored at nearly molar concentrations. We demonstrate that this extraordinary packaging is achieved by associating into Fuzzy Interacting Transient Zwitterion (FITZ) complexes upon binding the intrinsically disordered FITZ Anionic Partner (FITZAP). FITZ complexes form at intracellular ionic strengths and, upon exocytosis into seawater, lysin and sp18 are dispersed to drive fertilization. NMR analyses revealed that lysin uses a common molecular interface to bind both FITZAP and its egg receptor VERL. As sexual selection alters the lysin-VERL interface, FITZAP coevolves rapidly to maintain lysin binding. FITZAP-lysin interactions exhibit a similar species-specificity as lysin-VERL interactions. Thus, tethered molecular arms races driven by sexual selection can generally explain rapid sperm protein evolution.



2019 ◽  
Author(s):  
Damien B. Wilburn ◽  
Lisa M. Tuttle ◽  
Rachel E. Klevit ◽  
Willie J. Swanson

AbstractSexual selection can explain rapid evolution of fertilization proteins, yet sperm proteins evolve rapidly even if they are not directly involved in fertilization. Here we demonstrate that FITZAP, an intrinsically disordered sperm protein in the marine mollusk abalone, exploits differences in the intracellular and oceanic ionic environments to package the fertilization protein lysin at extraordinary concentrations inside sperm by forming Fuzzy Interacting Transient Zwitterion (FITZ) complexes. FITZAP binds lysin at the same protein interface as its egg receptor VERL, and as sexual selection rapidly alters the lysin-VERL interface, FITZAP coevolves rapidly to maintain lysin binding. Consequently, FITZAP-lysin interactions exhibit a similar species-specificity as lysin-VERL interactions. Thus, tethered molecular arms races driven by sexual selection can generally explain rapid sperm protein evolution.One Sentence SummaryStructural study of sperm proteins reveals a novel protein packaging/dispersion system embedded in a coevolutionary arms race.



2021 ◽  
Author(s):  
Katja R Kasimatis ◽  
Megan J Moerdyk-Schauwecker ◽  
Ruben Lancaster ◽  
Alexander Smith ◽  
John H Willis ◽  
...  

Sexual reproduction is a complex process that contributes to differences between the sexes and divergence between species. From a male's perspective, sexual selection can optimize reproductive success by acting on the variance in mating success (pre-insemination selection) as well as the variance in fertilization success (post-insemination selection). The balance between pre- and post-insemination selection has not yet been investigated using a strong hypothesis-testing framework that directly quantifies the effects of post-insemination selection on the evolution of reproductive success. Here we use experimental evolution of a uniquely engineered genetic system that allows sperm production to be turned off and on in obligate male-female populations of Caenorhabditis elegans. We show that enhanced post-insemination competition increases the efficacy of selection and surpasses pre-insemination sexual selection in driving a polygenic response in male reproductive success. We find that after 30 generations post-insemination selection increased male reproductive success by an average of 5- to 7-fold. Contrary to expectation, enhanced pre-insemination competition hindered selection and slowed the rate of evolution. Furthermore, we found that post-insemination selection resulted in a strong polygenic response at the whole-genome level. Our results demonstrate that post-insemination sexual selection plays a critical role in the rapid optimization of male reproductive fitness. Therefore, explicit consideration should be given to post-insemination dynamics when considering the population effects of sexual selection.



2009 ◽  
Vol 6 (1) ◽  
pp. 55-58 ◽  
Author(s):  
Andrew T. Kahn ◽  
Brian Mautz ◽  
Michael D. Jennions

Sexual selection is a major force behind the rapid evolution of male genital morphology among species. Most within-species studies have focused on sexual selection on male genital traits owing to events during or after copulation that increase a male's share of paternity. Very little attention has been given to whether genitalia are visual signals that cause males to vary in their attractiveness to females and are therefore under pre-copulatory sexual selection. Here we show that, on average, female eastern mosquitofish Gambusia holbrooki spent more time in association with males who received only a slight reduction in the length of the intromittent organ (‘gonopodium’) than males that received a greater reduction. This preference was, however, only expressed when females chose between two large males; for small males, there was no effect of genital size on female association time.



2020 ◽  
Vol 29 (8) ◽  
pp. 1476-1493 ◽  
Author(s):  
Ralph F. Schneider ◽  
Sina J. Rometsch ◽  
Julián Torres‐Dowdall ◽  
Axel Meyer


2018 ◽  
Author(s):  
Timothy L. Karr ◽  
Helen Southern ◽  
Matthew Rosenow ◽  
Toni I. Gossmann ◽  
Rhonda R. Snook

Polyandry drives postcopulatory sexual selection (PCSS), resulting in rapid evolution of male ejaculate traits. Critical to male and female fitness, the ejaculate is known to contain rapidly evolving seminal fluid proteins (SFPs) produced by specialized male secretory accessory glands. The evidence that rapid evolution of some SFPs is driven by PCSS, however, is indirect, based on either plastic responses to changes in the sexual selection environment or correlative macroevolutionary patterns. Moreover, such studies focus on SFPs that represent but a small component of the accessory gland proteome. Neither how SFPs function with other reproductive proteins, nor how PCSS influences the underlying secretory tissue adaptations and content of the accessory gland, has been addressed at the level of the proteome. Here we directly test the hypothesis that PCSS results in rapid evolution of the entire male accessory gland proteome and protein networks by taking a system-level approach, combining divergent experimental evolution of PCSS in Drosophila pseudoobscura (Dpse), high resolution mass spectrometry (MS) and proteomic discovery, bioinformatics and population genetic analyses. We demonstrate that PCSS influences the abundance of over 200 accessory gland proteins, including SFPs. A small but significant number of these proteins display molecular signatures of positive selection. Divergent PCSS also results in fundamental and remarkably compartmentalized evolution of accessory gland protein networks in which males subjected to strong PCSS invest in protein networks that serve to increase protein production whereas males subjected to relaxed PCSS alters protein networks involved in protein surveillance and quality. These results directly demonstrate that PCSS is a key evolutionary driver that shapes not only individual reproductive proteins, but rewires entire reproductive protein networks.The abbreviations used are:BLASTBasic Local Alignment Search ToolDpseDrosophila pseudoobscuraPCSSpostcopulatory sexual selectionSFPsseminal fluid proteinsDmelD. melanogasterSDSsodium dodecylsulfateSDS-PAGEsodium dodecylsulfate polyacrylamide gel electrophoresisMSmass spectrometryLC-MS/MSliquid chromatography-MS/MSAcgPaccessory gland proteomeFDRsFalse Discovery RatesAcgSaccessory gland secretomeexoPexoproteomeLFQlabel-free quantitationPpolyandryMmonandryGOgene ontologyCCcellular componentMFmolecular functionBPbiological processSTRINGSearch Tool for the Retrieval of Interacting Genes/ProteinsDIOPTDRSC Integrative Ortholog Prediction ToolsERendoplasmic reticulum



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