Socioecological and phylogenetic patterns in the chemical signals of strepsirrhine primates

Our understanding of chemical signals in mammals derives principally from studies in which researchers examine signal structure or function within a single species. Despite the unique information to be gained from applying comparable methods across multiple species, comparative studies of chemical signals are extremely limited. Here, we review the available literature on the evolution of chemosignals in male and female strepsirrhine primates (galagos, lorises and lemurs), all of which rely heavily on chemical communication. We draw from a few case studies, but focus our review on two comparative studies. In one, researchers examined the volatile chemical composition of urinary signals across 12 species representing most families within Strepsirrhini, including six 'urine-marking' species and six glandular or 'nonurine-marking' species. In the other, researchers examined the volatile chemical composition of glandular signals in eight Eulemur species differing in social or dominance structure. We highlight five findings. (1) Regardless of the scent source, chemical profiles differ substantially between species, providing reliable species 'scent signatures'. None the less, (2) urine markers express more compounds and have more distinguishable species scent signatures in their urine than do nonurine markers, suggesting specialization of function. Within Eulemur (3) chemical richness is greater in multimale-multifemale species than in pair-bonded species. Moreover, (4) whereas chemical richness of male signals is greater in sexually codominant species, chemical richness of female signals is greater in female-dominant species. Together, the findings from both comparative studies, coupled with case studies, suggest that signal richness is linked to some aspect of the focal species' socioecology. Lastly, (5) regardless of the scent source, strepsirrhine chemosignals evolve gradually over time, but at fast rates and homogeneously within different lineages. Comparative studies reveal patterns that cannot be detected from the single-species approach and are therefore critical for providing new insight into the function and evolution of olfactory signals

Two modes of input processing in relation to risk of sperm competition in mammals

Much research has been focused on the ‘output’ or response of males to particular risks of sperm competition (RSC). Lately, there has also been some interest on the types of information that males may use to assess RSC (RSC inputs). In contrast, there is a lack of studies on how males may process RSC inputs to generate such RSC outputs. Here we propose two modes of input processing (direct and indirect) and ways to test them in order to understand how a male may process and store RSC information. The direct mode of input processing predicts that a male may store RSC inputs through a physiological response, e.g., through a change in hormonal levels. As long as this response is active, the male will stay in a ‘RSC state’ and will produce an RSC output (e.g. high sperm investment) instead of a non-RSC output (e.g. relatively lower sperm investment) when he encounters a female. The indirect mode of input processing predicts that a male may store RSC inputs in his memory and retrieve such information later on to modify his output (e.g. sperm investment or copulatory behavior) accordingly. We use a multidisciplinary approach that should appeal to those researchers that seek to understand male’s adaptations to sperm competition at different levels. We believe that the testing of the hypotheses developed in this paper will lead to interesting findings and the development of new hypothese

Not all cities are the same: variation in animal phenotypes across cities within urban ecology studies

The sustained expansion of urban environments has been paralleled by an increase in the number of studies investigating the phenotypic changes of animals driven by urbanization. Most of these studies have been confined to only one urban center. However, as the types and strength of anthropogenic stressors differ across cities, a generalizable understanding of the effects of urbanization on urban-dwelling species can only be reached by comparing the responses of urban populations from the same species across more than one city. We conducted phylogenetic meta-analyses on data for animal species (including both invertebrates and vertebrates) for which measures about any morphological, physiological, or behavioral trait were reported for two or more cities. We found that morphological, physiological and behavioral traits of urban animals all differ similarly across cities, and that such phenotypic differences across cities increase as the more cities were investigated in any given study. We also found support for phenotypic differences across cities being more pronounced as the farther away cities are from each other. Our results clearly indicate that separate urban populations of the same species can diverge phenotypically, and support previous pleas from many researchers to conduct urban studies across several urban populations. We particularly recommend that future studies choose cities in different biomes, as urban adaptations may differ substantially in cities sited in different ecological matrices. Ultimately, a generalized knowledge about how organisms are affected by urbanization will only be possible when comprehensive biological patterns are similarly studied across separate and distinct cities

Differences in the fatty-acid composition of rodent spermatozoa are associated to levels of sperm competition.

Sperm competition is a prevalent phenomenon that drives the evolution of sperm function. High levels of sperm competition lead to increased metabolism to fuel higher sperm velocities. This enhanced metabolism can result in oxidative damage (including lipid peroxidation) and damage to the membrane. We hypothesized that in those species experiencing high levels of sperm competition there are changes in the fatty-acid composition of the sperm membrane that makes the membrane more resistant to oxidative damage. Given that polyunsaturated fatty acids (PUFAs) are the most prone to lipid peroxidation, we predicted that higher sperm competition leads to a reduction in the proportion of sperm PUFAs. In contrast, we predicted that levels of sperm competition should not affect the proportion of PUFAs in somatic cells. To test these predictions, we quantified the fatty-acid composition of sperm, testis and liver cells in four mouse species (genus Mus) that differ in their levels of sperm competition. Fatty-acid composition in testis and liver cells was not associated to sperm competition levels. However, in sperm cells, as predicted, an increase in sperm competition levels was associated with an increase in the proportion of saturated fatty-acids (the most resistant to lipid peroxidation) and by a concomitant decrease in the proportion of PUFAs. Two particular fatty acids were most responsible for this pattern (arachidonic acid and palmitic acid). Our findings thus indicate that sperm competition has a pervasive influence in the composition of sperm cells that ultimately may have important effects in sperm function

A comparison of human chorionic gonadotropin and luteinizing hormone releasing hormone on the induction of spermiation and amplexus in the American toad (Anaxyrus americanus).

BACKGROUND: Captive breeding programs for endangered amphibian species often utilize exogenous hormones for species that are difficult to breed. The purpose of our study was to compare the efficacy of two different hormones at various concentrations on sperm production, quantity and quality over time in order to optimize assisted breeding. METHODS: Male American toads (Anaxyrus americanus) were divided into three separate treatment groups, with animals in each group rotated through different concentrations of luteinizing hormone releasing hormone analog (LHRH; 0.1, 1.0, 4.0 and 32 micrograms/toad), human chorionic gonadotropin (hCG; 50, 100, 200, and 300 IU), or the control over 24 hours. We evaluated the number of males that respond by producing spermic urine, the sperm concentration, percent motility, and quality of forward progression. We also evaluated the effects of hCG and LHRH on reproductive behavior as assessed by amplexus. Data were analyzed using the Generalized Estimating Equations incorporating repeated measures over time and including the main effects of treatment and time, and the treatment by time interaction. RESULTS: The hormone hCG was significantly more effective at stimulating spermiation in male Anaxyrus americanus than LHRH and showed a dose-dependent response in the number of animals producing sperm. At the most effective hCG dose (300 IU), 100% of the male toads produced sperm, compared to only 35% for the best LHRH dose tested (4.0 micrograms). In addition to having a greater number of responders (P < 0.05), the 300 IU hCG treatment group had a much higher average sperm concentration (P < 0.05) than the treatment group receiving 4.0 micrograms LHRH. In contrast, these two treatments did not result in significant differences in sperm motility or quality of forward progressive motility. However, more males went into amplexus when treated with LHRH vs. hCG (90% vs. 75%) by nine hours post-administration. CONCLUSION: There is a clear dichotomy between the two hormones' physiological responses on gamete production and stimulation of amplexus. Understanding how these two hormones influence physiology and reproductive behaviors in amphibians will have direct bearing on establishing similar breeding protocols for endangered species

A cost for high levels of sperm competition in rodents: Increased sperm DNA fragmentation

Spermcompetition, a prevalent evolutionary process inwhich the spermatozoa of two or more males compete for the fertilization of the same ovum, leads to morphological and physiological adaptations, including increases in energetic metabolism that may serve to propel sperm faster but that may have negative effects onDNA integrity. SpermDNA damage is associated with reduced rates of fertilization, embryo and fetal loss, offspring mortality, and mutations leading to genetic disease. We tested whether high levels of sperm competition affect sperm DNA integrity. We evaluated sperm DNA integrity in 18 species of rodents that differ in their levels of spermcompetition using the spermchromatin structure assay. DNA integrity was assessed upon sperm collection, in response to incubation under capacitating or non-capacitating conditions, and after exposure to physical and chemical stressors. Sperm DNA was very resistant to physical and chemical stressors, whereas incubation in noncapacitating and capacitating conditions resulted in only a small increase in spermDNA damage. Importantly, levels of spermcompetition were positively associated with sperm DNA fragmentation across rodent species. This is the first evidence showing that high levels of sperm competition lead to an important cost in the form of increased sperm DNA damage.Peer Reviewe

Metabolic rate limits the effect of sperm competition on mammalian spermatogenesis.

Sperm competition leads to increased sperm production in many taxa. This response may result from increases in testes size, changes in testicular architecture or changes in the kinetics of spermatogenesis, but the impact of each one of these processes on sperm production has not been studied in an integrated manner. Furthermore, such response may be limited in species with low mass-specific metabolic rate (MSMR), i.e., large-bodied species, because they cannot process energy and resources efficiently enough both at the organismic and cellular levels. Here we compare 99 mammalian species and show that higher levels of sperm competition correlated with a) higher proportions of seminiferous tubules, b) shorter seminiferous epithelium cycle lengths (SECL) which reduce the time required to produce sperm, and c) higher efficiencies of Sertoli cells (involved in sperm maturation). These responses to sperm competition, in turn, result in higher daily sperm production, more sperm stored in the epididymides, and more sperm in the ejaculate. However, the two processes that require processing resources at faster rates (SECL and efficiency of Sertoli cells) only respond to sperm competition in species with high MSMR. Thus, increases in sperm production with intense sperm competition occur via a complex network of mechanisms, but some are constrained by MSMR

Molecular evolutionary characterization of a V1R subfamily unique to strepsirrhine primates.

Vomeronasal receptor genes have frequently been invoked as integral to the establishment and maintenance of species boundaries among mammals due to the elaborate one-to-one correspondence between semiochemical signals and neuronal sensory inputs. Here, we report the most extensive sample of vomeronasal receptor class 1 (V1R) sequences ever generated for a diverse yet phylogenetically coherent group of mammals, the tooth-combed primates (suborder Strepsirrhini). Phylogenetic analysis confirms our intensive sampling from a single V1R subfamily, apparently unique to the strepsirrhine primates. We designate this subfamily as V1Rstrep. The subfamily retains extensive repertoires of gene copies that descend from an ancestral gene duplication that appears to have occurred prior to the diversification of all lemuriform primates excluding the basal genus Daubentonia (the aye-aye). We refer to the descendent clades as V1Rstrep-α and V1Rstrep-β. Comparison of the two clades reveals different amino acid compositions corresponding to the predicted ligand-binding site and thus potentially to altered functional profiles between the two. In agreement with previous studies of the mouse lemur (genus, Microcebus), the majority of V1Rstrep gene copies appear to be intact and under strong positive selection, particularly within transmembrane regions. Finally, despite the surprisingly high number of gene copies identified in this study, it is nonetheless probable that V1R diversity remains underestimated in these nonmodel primates and that complete characterization will be limited until high-coverage assembled genomes are available

Characterizing the scent and chemical composition of Panthera leo marking fluid using solid-phase microextraction and multidimensional gas chromatography–mass spectrometry-olfactometry

Lions (Panthera leo) use chemical signaling to indicate health, reproductive status, and territorial ownership. To date, no study has reported on both scent and composition of marking fluid (MF) from P. leo. The objectives of this study were to: 1) develop a novel method for simultaneous chemical and scent identification of lion MF in its totality (urine + MF), 2) identify characteristic odorants responsible for the overall scent of MF as perceived by human panelists, and 3) compare the existing library of known odorous compounds characterized as eliciting behaviors in animals in order to understand potential functionality in lion behavior. Solid-phase microextraction and simultaneous chemical-sensory analyses with multidimensional gas-chromatography-mass spectrometry-olfactometry improved separating, isolating, and identifying mixed (MF, urine) compounds versus solvent-based extraction and chemical analyses. 2,5-Dimethylpyrazine, 4-methylphenol, and 3-methylcyclopentanone were isolated and identified as the compounds responsible for the characteristic odor of lion MF. Twenty-eight volatile organic compounds (VOCs) emitted from MF were identified, adding a new list of compounds previously unidentified in lion urine. New chemicals were identified in nine compound groups: ketones, aldehydes, amines, alcohols, aromatics, sulfur-containing compounds, phenyls, phenols, and volatile fatty acids. Twenty-three VOCs are known semiochemicals that are implicated in attraction, reproduction, and alarm-signaling behaviors in other species