Maternal food restriction during pregnancy affects offspring development and swimming performance in a placental live-bearing fish

How pregnant mothers allocate limited resources to different biological functions such as maintenance, somatic growth, and reproduction can have profound implications for early life development and survival of offspring. Here we examined the effects of maternal food restriction during pregnancy on offspring in the matrotrophic (i.e. mother-nourishment throughout gestation) live-bearing fish species Phalloptychus januarius (Poeciliidae). We fed pregnant females either with a ‘low-food’ or ‘high-food’ ration for six weeks and quantified the consequences for offspring size and body fat at birth and one week after birth. We further measured fast-start escape performance of offspring at birth, as well as swimming kinematics during prey capture at zero, two, and seven days after birth. We found that the length of maternal food restriction during pregnancy negatively affected offspring dry mass and lean dry mass at birth, as well as body fat gain during the first week after birth. Moreover, it impacted the locomotor performance of offspring during prey capture at, and during the first week after, birth. We did not observe an effect of food restriction on fast-start escape performance of offspring. Our study suggests that matrotrophic poeciliid fish are maladapted to unpredictably fluctuating resource environments, because sudden reductions in maternal food availability during pregnancy result in smaller offspring with slower postnatal body fat gain and an inhibition of postnatal improving swimming skills during feeding, potentially leading to lower competitive abilities after birth.

Sex Chromosome Heteromorphism and the Fast-X Effect in Poeciliids

An accelerated rate of sequence evolution on the X chromosome compared to autosomes, known as Fast-X evolution, has been observed in a range of heteromorphic sex chromosomes. However, it remains unclear how early in the process of sex chromosome differentiation the Fast-X effect becomes detectible. Recently, we uncovered an extreme variation in sex chromosome heteromorphism across Poeciliid fish species. The common guppy, Poecilia reticulata, Endler’s guppy, P. wingei, and the swamp guppy, P. picta, appear to share the same XY system and exhibit a remarkable range of heteromorphism. The sex chromosome system is absent in recent outgroups, including P. latipinna and Gambusia holbrooki. We combined analyses of sequence divergence and polymorphism data across Poeciliids to investigate X chromosome evolution as a function of hemizygosity and reveal the causes for Fast-X effects. Consistent with the extent of Y degeneration in each species, we detect higher rates of divergence on the X relative to autosomes and a strong Fast-X effect in P. picta, while no change in the rate of evolution of X-linked relative to autosomal genes in P. reticulata. In P. wingei, the species with intermediate sex chromosome differentiation, we see an increase in the rate of nonsynonymous substitutions on the older stratum of divergence only. We also use our comparative approach to test different models for the origin of the sex chromosomes in this clade. Taken together, our study reveals an important role of hemizygosity in Fast-X and suggests a single, recent origin of the sex chromosome system in this clade.

The evolution of a placenta is not linked to increased brain size in poeciliid fishes

ABSTRACTMaternal investment is considered to have a direct influence on the size of energetically costly organs, including the brain. In placental organisms, offspring are supplied with nutrients during pre-natal development, potentially modulating brain size. However, the coevolution of the placenta and brain size remains largely unknown in non-mammalian taxa. Here, using eight poeciliid fish species, we test if species with placental structures invest more resources into offspring brain development than species without placental structures. We predict that matrotrophy may entail higher nutrient provisioning rates to the developing embryo than lecithotrophy, resulting in larger brain sizes in offspring of matrotrophic species, and that a relatively larger part of the total brain growth would occur at younger ages (leading to a shallower ontogenetic brain size allometry). We took non-invasive brain size measurements during the first four weeks of life, and compared these to somatic growth measurements. Contrary to our expectations, we did not find any differences in brain size between the two maternal strategies. Furthermore, we did not find any differences in how relative brain size changed over ontogenetic development, between placental and non-placental species. In contrast to the marsupial/placental transition, the species investigated here only exhibit pre-natal provisioning, which may reduce the potential for maternal investment into brain size. Consequently, our results suggest that coevolution between placental structures and juvenile brain size is not a general pattern.

Chromosome-level genome assembly of the female western mosquitofish (Gambusia affinis)

Background The western mosquitofish (Gambusia affinis) is a sexually dimorphic poeciliid fish known for its worldwide biological invasion and therefore an important research model for studying invasion biology. This organism may also be used as a suitable model to explore sex chromosome evolution and reproductive development in terms of differentiation of ZW sex chromosomes, ovoviviparity, and specialization of reproductive organs. However, there is a lack of high-quality genomic data for the female G. affinis; hence, this study aimed to generate a chromosome-level genome assembly for it. Results The chromosome-level genome assembly was constructed using Oxford nanopore sequencing, BioNano, and Hi-C technology. G. affinis genomic DNA sequences containing 217 contigs with an N50 length of 12.9 Mb and 125 scaffolds with an N50 length of 26.5 Mb were obtained by Oxford nanopore and BioNano, respectively, and the 113 scaffolds (90.4% of scaffolds containing 97.9% nucleotide bases) were assembled into 24 chromosomes (pseudo-chromosomes) by Hi-C. The Z and W chromosomes of G. affinis were identified by comparative genomic analysis of female and male G. affinis, and the mechanism of differentiation of the Z and W chromosomes was explored. Combined with transcriptome data from 6 tissues, a total of 23,997 protein-coding genes were predicted and 23,737 (98.9%) genes were functionally annotated. Conclusions The high-quality female G. affinis reference genome provides a valuable omics resource for future studies of comparative genomics and functional genomics to explore the evolution of Z and W chromosomes and the reproductive developmental biology of G. affinis.

Expression analyses of cave mollies ( Poecilia mexicana ) reveal key genes involved in the early evolution of eye regression

Eye regression occurs across cave-dwelling populations of many species and is often coupled with a decrease or loss in eye function. Teleost fishes are among the few vertebrates to undergo widespread colonization of caves and often exhibit eye regression with blindness. Cave populations of the poeciliid fish Poecilia mexicana (cave molly) exhibit reduced—albeit functional—eyes, offering the opportunity to investigate partial eye regression. We sequenced eye transcriptomes of cave and surface populations of P. mexicana to identify differentially expressed genes that potentially underlie eye regression in cave mollies. We identified 28 significantly differentially expressed genes, 20 of which were directly related to light sensitivity, eye structure and visual signaling. Twenty-six of these genes were downregulated in cave compared to surface populations. Functional enrichment analysis revealed eye-related gene ontologies that were under-represented in cave mollies. In addition, a set of co-expressed genes related to vision and circadian rhythm was correlated with habitat type (cave versus surface). Our study suggests that differential gene expression plays a key role in the beginning evolutionary stages of eye regression in P. mexicana , shedding further light on regressive evolution in cavefish.

Extreme fertilization bias towards freshly inseminated sperm in a species exhibiting prolonged female sperm storage

The storage of sperm by females across successive reproductive cycles is well documented in internal fertilizers, yet the fate of stored sperm when they compete with ‘new’ sperm to fertilize a female's eggs has rarely been considered. This gap in our understanding is likely due to the logistical difficulties of controlling behavioural interactions during or after mating, which in turn may influence how many sperm are inseminated and how stored sperm are ultimately used during successive bouts of sperm competition with freshly inseminated sperm. Here, we use artificial insemination (AI) in guppies ( Poecilia reticulata ), a polyandrous live-bearing poeciliid fish exhibiting prolonged sperm storage by females, to overcome these challenges. The use of AI enables us to control potential differential maternal effects (e.g. behaviourally mediated cryptic female choice) and specifically test for post-copulatory paternity biases that favour either stored or fresh sperm when they compete to fertilize eggs. Our paternity analyses revealed the almost complete dominance of freshly inseminated sperm over stored sperm, supporting previous studies reporting similar patterns following natural matings across successive brood cycles. However, our use of AI, which excluded behavioural interactions between males and females, most likely generated a far stronger pattern of fresh sperm precedence compared with those reported in previous studies, possibly implicating ‘cryptic' forms of selection by females that may sometimes bolster the success of stored sperm.