A 24-Year Record of Female Reproductive Dynamics in Two Sympatric Mouse Lemur Species in Northwestern Madagascar

Seasonal reproduction is widespread among primates but the degree of reproductive synchrony and plasticity can vary, even between closely related species. This study compares the dynamics of female reproductive seasonality in two mouse lemur species, Microcebus murinus and M. ravelobensis, in Ankarafantsika National Park, Madagascar, across 24 years. We collected 4321 records of female reproductive state from 1033 individual females (319 M. murinus, 714 M. ravelobensis). The analyses revealed disparate reproductive schedules: While female M. murinus showed high degrees of reproductive synchrony throughout all years, leading to the production of two successive litters, the seasonal onset of estrus (= reproductive activation) in female M. ravelobensis was more flexible than in M. murinus, starting 2-4 weeks earlier, varying by up to 4 weeks between years, and being less synchronized. M. ravelobensis females became reproductively active later in years with more rainfall, in particular rain in February, but the timing of reproductive activation was not related to differences in temperatures. The likelihood of early conception was significantly lower in M. ravelobensis than in M. murinus. This was partly due to delayed reproductive activation in young animals, and a lower likelihood of early conception for females with low body mass in M. ravelobensis. Our results suggest high, adaptive reproductive plasticity in M. ravelobensis that may enable individuals to respond flexibly to yearly environmental changes and expand the reproductive period under favorable conditions. These species differences in reproductive schedules may be the result of the divergent evolutionary histories of the two mouse lemur species in different parts of Madagascar.

Functional differences between TSHR alleles associate with variation in spawning season in Atlantic herring

The underlying molecular mechanisms that determine long day versus short day breeders remain unknown in any organism. Atlantic herring provides a unique opportunity to examine the molecular mechanisms involved in reproduction timing, because both spring and autumn spawners exist within the same species. Although our previous whole genome comparisons revealed a strong association of TSHR alleles with spawning seasons, the functional consequences of these variants remain unknown. Here we examined the functional significance of six candidate TSHR mutations strongly associated with herring reproductive seasonality. We show that the L471M missense mutation in the spring-allele causes enhanced cAMP signaling. The best candidate non-coding mutation is a 5.2 kb retrotransposon insertion upstream of the TSHR transcription start site, near an open chromatin region, which is likely to affect TSHR expression. The insertion occurred prior to the split between Pacific and Atlantic herring and was lost in the autumn-allele. Our study shows that strongly associated coding and non-coding variants at the TSHR locus may both contribute to the regulation of seasonal reproduction in herring.

Seasonal Effect on Developmental Competence, Oxidative Status and Tubulin Assessment of Prepubertal Ovine Oocyte

The reproductive seasonality of domestic animals is often manipulated in order to have more reproductive periods for commercial purposes related to the production of milk and meat. It is scientifically proven that such an alteration of the reproductive activity in sheep entails a deterioration in oocyte quality, leading to an inability to generate embryos. Since oocytes obtained from prepubertal ewes can be incorporated into an in vitro embryo production system and considering that their quality is crucial to the success of in vitro procedures, the aim of this work was to investigate the effect of seasons on the quality of prepubertal ovine oocytes collected in autumn and spring. Ovaries were collected from a local slaughterhouse from 30–40-day-old suckling lambs during both seasons. Following 24 h of in vitro maturation, oocytes developmental competence, reactive oxygen species (ROS) intracellular levels, and mitochondrial activity were evaluated, and a tubulin assessment was performed. The results on embryo production, as a percentage of first divisions and number of blastocysts obtained, were significantly higher in oocytes collected in the spring. Mitochondrial activity in oocytes was higher, and ROS production significantly lower, in spring than in autumn. Tubulin PTMs (tyrosinated and acetylated α-tubulin) showed a higher immunoreactivity in oocytes collected in spring compared with autumn sampling. Our data showed that seasons may affect the developmental competence, energetic status, and tubulin assessment of oocytes recovered from prepubertal ewes. Therefore, special care should be taken when choosing the period of the year for prepuberal ovine oocytes collection aimed at in vitro embryo reproduction programs.

Birth timing generates reproductive trade-offs in a non-seasonal breeding primate

The evolutionary benefits of reproductive seasonality are often measured by a single-fitness component, namely offspring survival. Yet different fitness components may be maximized by different birth timings. This may generate fitness trade-offs that could be critical to understanding variation in reproductive timing across individuals, populations and species. Here, we use long-term demographic and behavioural data from wild chacma baboons ( Papio ursinus ) living in a seasonal environment to test the adaptive significance of seasonal variation in birth frequencies. We identify two distinct optimal birth timings in the annual cycle, located four-month apart, which maximize offspring survival or minimize maternal interbirth intervals (IBIs), by respectively matching the annual food peak with late or early weaning. Observed births are the most frequent between these optima, supporting an adaptive trade-off between current and future reproduction. Furthermore, infants born closer to the optimal timing favouring maternal IBIs (instead of offspring survival) throw more tantrums, a typical manifestation of mother–offspring conflict. Maternal trade-offs over birth timing, which extend into mother–offspring conflict after birth, may commonly occur in long-lived species where development from birth to independence spans multiple seasons. Our findings therefore open new avenues to understanding the evolution of breeding phenology in long-lived animals, including humans.

Habitat characteristics and life history explain reproductive seasonality in lagomorphs

Lagomorphs show extensive seasonal variation in their reproduction. However, the factors causing this large variation have so far mostly been investigated intraspecifically and therefore provide only some exemplary comparisons of lagomorph reproductive seasonality. The present study applies both a categorical description (birth season categories 1–5) and a quantitative measure (birth season length in months) to summarize the degree of birth seasonality in the wild of 69 lagomorph species. Using a comparative approach, I tested the influence of 13 factors, comprising six habitat, five life history and two allometric variables on birth season length in lagomorphs. Leporids mainly show non-seasonal birthing patterns with high intraspecific variation. Their opportunistic breeding strategy with high reproductive output and their large distribution areas across wide latitude and elevation ranges might be the reasons for this finding. Ochotonids reproduce strictly seasonally, likely because they live at northern latitudes, are high-altitude specialists, and occur in limited distribution areas. The most important factors associated with variation in lagomorph birth seasonality are mid-latitude, mean annual temperature and precipitation of a species’ geographical range and life history adaptations including fewer but larger litters in seasonal habitats. Birth seasons become shorter with increasing latitude, colder temperatures, and less precipitation, corresponding to the decreasing length of optimal environmental conditions. Leporid species with shorter breeding seasons force maternal resources into few large litters to maximise reproductive output while circumstances are favourable. Since allometric variables were only weakly associated with reproductive seasonality, life history adaptations and habitat characteristics determine birth seasonality in Lagomorpha.

Genome-Wide Association Study Demonstrates the Role Played by the CD226 Gene in Rasa Aragonesa Sheep Reproductive Seasonality

A genome-wide association study (GWAS) was used to identify genomic regions influencing seasonality reproduction traits in Rasa Aragonesa sheep. Three traits associated with either ovarian function based on blood progesterone levels (total days of anoestrus and progesterone cycling months) or behavioral signs of oestrous (oestrous cycling months) were studied. The GWAS included 205 ewes genotyped using the 50k and 680k Illumina Ovine Beadchips. Only one SNP associated with the progesterone cycling months overcame the genome-wide significance level (rs404991855). Nine SNPs exhibited significant associations at the chromosome level, being the SNPs rs404991855 and rs418191944, that are located in the CD226 molecule (CD226) gene, associated with the three traits. This gene is related to reproductive diseases. Two other SNPs were located close to the neuropeptide Y (NPY) gene, which is involved in circadian rhythms. To validate the GWAS, partial characterization of both genes by Sanger sequencing, and genotyping of two synonymous and two nonsynonymous SNPs in the NPY and CD226 genes, respectively, were performed. SNP association analysis showed that only SNP rs404360094 in the exon 3 of the CD226 gene, which produces an amino acid substitution from asparagine (uncharged polar) to aspartic acid (acidic), was associated with the three seasonality traits. Our results suggest that the CD226 gene may be involved in the reproductive seasonality in Rasa Aragonesa.

Evolutionary determinants of non-seasonal breeding in wild chacma baboons

ABSTRACTAnimal reproductive phenology varies from strongly seasonal to non-seasonal, sometimes among closely related or sympatric species. While the extent of reproductive seasonality is often attributed to environmental seasonality, this fails to explain many cases of non-seasonal breeding in seasonal environments. We investigated the evolutionary determinants of non-seasonal breeding in a wild primate, the chacma baboon (Papio ursinus), living in a seasonal environment with high climatic unpredictability. We tested three hypotheses proposing that non-seasonal breeding has evolved in response to (1) climatic unpredictability, (2) reproductive competition between females favouring birth asynchrony, and (3) individual, rank-dependent variations in optimal reproductive timing. We found strong support for an effect of reproductive asynchrony modulated by rank: (i) birth synchrony is costly to subordinate females, lengthening their interbirth intervals, and (ii) females delay their reproductive timings (fertility periods and conceptions) according to other females in the group to stagger conceptions. These results indicate that reproductive competition generates reproductive asynchrony, weakening the intensity of reproductive seasonality at the population level. This study emphasizes the importance of sociality in mediating the evolution of reproductive phenology in gregarious organisms, a result of broad significance for understanding key demographic parameters driving population responses to increasing climatic fluctuations.

Reproductive Seasonality Affects In Vitro Embryo Production Outcomes in Adult Goats

Reproductive seasonality may have a considerable influence on the efficiency of assisted reproductive technologies in seasonal species. This study evaluated the effect of season on cleavage, blastocyst rates and quality of in vitro produced (IVP) goat embryos. In total, 2348 cumulus–oocyte complexes (COCs) were recovered from slaughterhouse ovaries and subjected to the same IVP system throughout 1.5 years (49 replicates). The odds ratio (OR) among seasons was calculated from values of cleavage and blastocyst rates in each season. Cleavage rate was lower (p < 0.05) in spring (anestrus), in comparison with either autumn (peak of breeding season) or summer, while the winter had intermediate values. Furthermore, lower OR of cleavage was observed in spring. Blastocyst formation rate (from initial number of COCs) was higher (p < 0.05) in autumn (52 ± 2.5%) when compared with the other seasons (combined rates: 40 ± 1.9%). Moreover, its OR was higher (p < 0.05) in autumn compared to all other seasons and impaired in the spring compared to winter (OR: 0.54) and summer (OR: 0.48). Embryo hatchability and blastocyst cell number were similar (p > 0.05) among seasons. In conclusion, the breeding season leads to improved oocyte developmental competence, resulting in higher cleavage and blastocyst yield, whereas embryo quality remained similar throughout the years.