Loveland, J. L. | bioRxiv Science

bioRxiv2023

Sperm traits of the three genetic morphs in the ruff sandpiper

BackgroundThe ruff sandpiper Calidris pugnax is a Palearctic lekking shorebird with three genetic morphs determined by an autosomal inversion. Male morphs differ strikingly in body size, ornaments, endocrinology and mating behavior. Aggressive Independents represent the ancestral haplotype, while female-mimicking Faeders and semi-cooperative Satellites are the inverted haplotypes. Because one inversion breakpoint is homozygous lethal, the inverted haplotypes cannot recombine and are expected to accumulate deleterious mutations. The inversion regions also harbor genes involved in spermatogenesis. However, it remains unknown whether the genetic differences between the morphs also translate into differences in sperm traits. Here, we use a captive-bred population of ruffs to compare sperm swimming speed and morphology among the morphs. ResultsRuff sperm morphologically resembled those of passerines, but moved differently, vibrating from side to side while slowly moving forward, rather than rotating while moving forward. Faeder sperm moved the slowest, which is consistent with the prediction of genetic deterioration over time. However, against expectation, sperm of Independents did not seem to be of the highest quality, i.e., their sperm were not the fastest nor the least variable, and they had sperm with the shortest tail and midpiece. Although the midpiece contains the energy-producing mitochondria, sperm midpiece length was not associated with sperm swimming speed. Instead, two of three velocity metrics weakly positively correlated with head length (absolute and relative). ConclusionsThe three genetically determined ruff morphs showed subtle differences in swimming speed and in the length of some sperm components. However, the between-morph differences in sperm swimming speed were not linked to the differences in morphology. We conclude that there is at best limited evidence for lower-quality sperm in the morphs that carry the inversion, and suggest that the potential for the evolution of morph-specific sperm adaptations may be limited in this system. Lay SummaryThe ruff sandpiper is a shorebird that exhibits three genetically distinct types of males, which differ markedly in body size, ornaments, hormones, and mating behavior. Aggressive Independents represent the type that evolved first. Semi-cooperative Satellites and female-mimicking Faeders evolved later through a specific type of genetic rearrangement called an inversion, in which a segment of a chromosome reversed in orientation. Due to the nature of this inversion, Satellite and Faeder chromosomes are expected to deteriorate over time. However, it remains unclear whether the genetic differences between these morphs, which affect physiological and behavioral traits, also translate into differences in sperm traits. We used a captive population of ruffs to compare sperm swimming speed and length measurements between the three types of males. Faeder sperm was the slowest, which is consistent with expectations based on genetic deterioration over time. However, against our expectations, the sperm of Independents does not appear to have better performance characteristics. Although the midpiece of a sperm is responsible for energy production, the length of the midpiece did not relate to sperm swimming speed.

evolutionary biology↗

bioRxiv2020

Functional differences in the hypothalamic-pituitary-gonadal axis are associated with alternative reproductive tactics based on an inversion polymorphism

The evolution of social behavior depends on genetic changes, yet, how genomic variation manifests itself in behavioral diversity is still largely unresolved. Chromosomal inversions can play a pivotal role in producing distinct behavioral phenotypes, in particular, when inversion genes are functionally associated with hormone synthesis and signaling. Male Ruffs exhibit alternative reproductive tactics (ARTs) with an autosomal inversion determining two alternative morphs with clear behavioral and hormonal differences to the ancestral morph. We investigated hormonal and transcriptomic differences in the pituitary and gonads. Using a GnRH challenge, we found that the ability to synthesize testosterone in inversion carriers is severely constrained, whereas the synthesis of androstenedione, a testosterone precursor, is not. Inversion morphs were able to produce a transient increase in androstenedione following the GnRH injection, supporting the view that pituitary sensitivity to GnRH is comparable to that of the ancestral morph. We then performed gene expression analyses in a second set of untreated birds and found no evidence of alterations to pituitary sensitivity, gonadotropin production or gonad sensitivity to luteinizing hormone or follicle-stimulating hormone across morphs. Inversion morphs also showed reduced progesterone receptor expression in the pituitary. Strikingly, in the gonads, inversion morphs over-expressed STAR, a gene that is located outside of the inversion and responsible for providing the cholesterol substrate required for the synthesis of sex hormones. In conclusion, our results suggest that the gonads determine morph-specific differences in hormonal regulation.

physiology↗