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1. Vertically transmitted microbiome protects eggs from fungal infection and egg failure

   https://doi.org/10.1186/s42523-021-00104-5  

   Bunker, M. E.; Elliott, G.; Heyer-Gray, H.; Martin, M. O.; Arnold, A. E.; Weiss, S. L. (December 2021, Animal Microbiome)

   Abstract Background Beneficial microbes can be vertically transmitted from mother to offspring in many organisms. In oviparous animals, bacterial transfer to eggs may improve egg success by inhibiting fungal attachment and infection from pathogenic microbes in the nest environment. Vertical transfer of these egg-protective bacteria may be facilitated through behavioral mechanisms such as egg-tending, but many species do not provide parental care. Thus, an important mechanism of vertical transfer may be the passage of the egg through the maternal cloaca during oviposition itself. In this study, we examined how oviposition affects eggshell microbial communities, fungal attachment, hatch success, and offspring phenotype in the striped plateau lizard, Sceloporus virgatus , a species with no post-oviposition parental care. Results Relative to dissected eggs that did not pass through the cloaca, oviposited eggs had more bacteria and fewer fungal hyphae when examined with a scanning electron microscope. Using high throughput Illumina sequencing, we also found a difference in the bacterial communities of eggshells that did and did not pass through the cloaca, and the diversity of eggshell communities tended to correlate with maternal cloacal diversity only for oviposited eggs, and not for dissected eggs, indicating that vertical transmission of microbes is occurring. Further, we found that oviposited eggs had greater hatch success and led to larger offspring than those that were dissected. Conclusions Overall, our results indicate that female S. virgatus lizards transfer beneficial microbes from their cloaca onto their eggs during oviposition, and that these microbes reduce fungal colonization and infection of eggs during incubation and increase female fitness. Cloacal transfer of egg-protective bacteria may be common among oviparous species, and may be especially advantageous to species that lack parental care. 

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2. Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata

   https://doi.org/10.1002/ece3.5580  

   Jennings, Emily C.; Korthauer, Matthew W.; Hamilton, Trinity L.; Benoit, Joshua B. (August 2019, Ecology and Evolution)

   Abstract The vertical transmission of microbes from mother to offspring is critical to the survival, development, and health of animals. Invertebrate systems offer unique opportunities to conduct studies on microbiome‐development‐reproduction dynamics since reproductive modes ranging from oviparity to multiple types of viviparity are found in these animals. One such invertebrate is the live‐bearing cockroach,Diploptera punctata. Females carry embryos in their brood sac, which acts as the functional equivalent of the uterus and placenta. In our study, 16S rRNA sequencing was used to characterize maternal and embryonic microbiomes as well as the development of the whole‐body microbiome across nymphal development. We identified 50 phyla and 121 classes overall and found that mothers and their developing embryos had significantly different microbial communities. Of particular interest is the notable lack of diversity in the embryonic microbiome, which is comprised exclusively of Blattabacteria, indicating microbial transmission of only this symbiont during gestation. Our analysis of postnatal development reveals that significant amounts of non‐Blattabacteria species are not able to colonize newbornD. punctatauntil melanization, after which the microbial community rapidly and dynamically diversifies. While the role of these microbes during development has not been characterized, Blattabacteria must serve a critical role providing specific micronutrients lacking in milk secretions to the embryos during gestation. This research provides insight into the microbiome development, specifically with relation to viviparity, provisioning of milk‐like secretions, and mother–offspring interactions during pregnancy. 

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3. Cloacal microbiomes of sympatric and allopatric Sceloporus lizards vary with environment and host relatedness

   https://doi.org/10.1371/journal.pone.0279288  

   Bunker, Marie E.; Weiss, Stacey L. (December 2022, PLOS ONE)

   Ruiz-Rodriguez, Magdalena (Ed.)

   Animals and their microbiomes exert reciprocal influence; the host’s environment, physiology, and phylogeny can impact the composition of the microbiome, while the microbes present can affect host behavior, health, and fitness. While some microbiomes are highly malleable, specialized microbiomes that provide important functions can be more robust to environmental perturbations. Recent evidence suggests Sceloporus virgatus has one such specialized microbiome, which functions to protect eggs from fungal pathogens during incubation. Here, we examine the cloacal microbiome of three different Sceloporus species (spiny lizards; Family Phrynosomatidae)– Sceloporus virgatus , Sceloporus jarrovii , and Sceloporus occidentalis . We compare two species with different reproductive modes (oviparous vs. viviparous) living in sympatry: S . virgatus and S . jarrovii . We compare sister species living in similar habitats (riparian oak-pine woodlands) but different latitudes: S . virgatus and S . occidentalis . And, we compare three populations of one species ( S . occidentalis ) living in different habitat types: beach, low elevation forest, and the riparian woodland. We found differences in beta diversity metrics between all three comparisons, although those differences were more extreme between animals in different environments, even though those populations were more closely related. Similarly, alpha diversity varied among the S . occidentalis populations and between S . occidentalis and S . virgatus , but not between sympatric S . virgatus and S . jarrovii . Despite these differences, all three species and all three populations of S . occcidentalis had the same dominant taxon, Enterobacteriaceae . The majority of the variation between groups was in low abundance taxa and at the ASV level; these taxa are responsive to habitat differences, geographic distance, and host relatedness. Uncovering what factors influence the composition of wild microbiomes is important to understanding the ecology and evolution of the host animals, and can lead to more detailed exploration of the function of particular microbes and the community as a whole. 

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4. Recovered microbiome of an oviparous lizard differs across gut and reproductive tissues, cloacal swabs, and faeces

   https://doi.org/10.1111/1755-0998.13573  

   Bunker, Marie E.; Martin, Mark O.; Weiss, Stacey L. (December 2021, Molecular Ecology Resources)

   Abstract Microbial diversity and community function are related, and can be highly specialized in different gut regions. The cloacal microbiome ofSceloporus virgatusfemales provides antifungal protection to eggshells, a specialized function that suggests a specialized microbiome. Here, we describe the cloacal, intestinal, and oviductal microbiome fromS.virgatusgravid females, adding to growing evidence of microbiome localization in reptiles and other taxa. We further assessed whether common methods for sampling gastrointestinal (GI) microbes – cloacal swabs and faeces – provide accurate representations of these microbial communities. We found that different regions of the gut had unique microbial communities. The cloacal microbiome showed extreme specialization averaging 99% Proteobacteria (Phylum) and 83%Enterobacteriacaea(Family).Enterobacteriacaeadecreased up the GI and reproductive tracts. Cloacal swabs recovered communities similar to that of lower intestine and cloacal tissues. In contrast, faecal samples had much higher diversity and a distinct composition (common Phyla: 62% Firmicutes, 18% Bacteroidetes, 10% Proteobacteria; common families: 39%Lachnospiraceae, 11%Ruminococcaceae, 11%Bacteroidaceae) relative to all gut regions. The common families in faecal samples made up <1% of cloacal tissue samples, increasing to 43% at the upper intestine. Similarly, the common families in gut tissue (EnterobacteriaceaeandHelicobacteraceae) made up <1% of the faecal microbiome. Further, we found that cloacal swabs taken shortly after defaecation may be contaminated with faecal matter. Our results serve as a caution against using faeces as a proxy for GI microbes, and may help explain high between‐sample variation seen in some studies using cloacal swabs. 

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5. The influence of incubation temperature on offspring traits varies across northern and southern populations of the American alligator ( Alligator mississippiensis )

   https://doi.org/10.1002/ece3.10915  

   Smaga, Christopher R; Bock, Samantha L; Johnson, Josiah M; Rainwater, Thomas; Singh, Randeep; Deem, Vincent; Letter, Andrew; Brunell, Arnold; Parrott, Benjamin B (February 2024, Ecology and Evolution)

   Abstract Maternal provisioning and the developmental environment are fundamental determinants of offspring traits, particularly in oviparous species. However, the extent to which embryonic responses to these factors differ across populations to drive phenotypic variation is not well understood. Here, we examine the contributions of maternal provisioning and incubation temperature to hatchling morphological and metabolic traits across four populations of the American alligator (Alligator mississippiensis), encompassing a large portion of the species' latitudinal range. Our results show that whereas the influence of egg mass is generally consistent across populations, responses to incubation temperature show population‐level variation in several traits, including mass, head length, head width, and residual yolk mass. Additionally, the influence of incubation temperature on developmental rate is greater at northern populations, while the allocation of maternal resources toward fat body mass is greater at southern populations. Overall, our results suggest that responses to incubation temperature, relative to maternal provisioning, are a larger source of interpopulation phenotypic variation and may contribute to the local adaptation of populations. 

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