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The short-beaked echidna is an iconic Australian animal and the most-widespread native mammal, inhabiting diverse environments. The cryptic nature of echidnas has limited research into their ecology in most areas; however, from the well-researched and endangered Kangaroo Island echidna population, we understand that the threats include habitat loss, roads, and invasive species. To obtain more information about echidnas Australia-wide, we established the Echidna Conservation Science Initiative (EchidnaCSI) citizen science project. EchidnaCSI calls on members of the public to submit photographs of wild echidnas and learn to identify and collect echidna scats for molecular analysis. To facilitate participation, we developed a smartphone application as well as ongoing social and traditional media activities and community events. In 3 y, more than 9,000 members of the public have downloaded the EchidnaCSI app, collecting 400 scats and submitting over 8,000 sightings of echidnas from across Australia. A subset of submitted scat samples were subjected to DNA extraction and PCR, which validated the approach of using citizen science for scat collection and viability for molecular analysis. To assess the impact of the project through public participation, we surveyed our participants (n = 944) to understand their demographics and motivations for engagement. Survey results also revealed that EchidnaCSI served as a gateway into citizen science more generally for many participants. EchidnaCSI demonstrates the potential for using citizen science approaches to collect high-quality data and material from a cryptic species over a very large geographic area and the considerable engagement value of citizen science research.

Egg-laying mammals (monotremes) are the only extant mammalian outgroup to therians (marsupial and eutherian animals) and provide key insights into mammalian evolution 1 , 2 . Here we generate and analyse reference genomes of the platypus ( Ornithorhynchus anatinus ) and echidna ( Tachyglossus aculeatus ), which represent the only two extant monotreme lineages. The nearly complete platypus genome assembly has anchored almost the entire genome onto chromosomes, markedly improving the genome continuity and gene annotation. Together with our echidna sequence, the genomes of the two species allow us to detect the ancestral and lineage-specific genomic changes that shape both monotreme and mammalian evolution. We provide evidence that the monotreme sex chromosome complex originated from an ancestral chromosome ring configuration. The formation of such a unique chromosome complex may have been facilitated by the unusually extensive interactions between the multi-X and multi-Y chromosomes that are shared by the autosomal homologues in humans. Further comparative genomic analyses unravel marked differences between monotremes and therians in haptoglobin genes, lactation genes and chemosensory receptor genes for smell and taste that underlie the ecological adaptation of monotremes. New reference genomes of the two extant monotreme lineages (platypus and echidna) reveal the ancestral and lineage-specific genomic changes that shape both monotreme and mammalian evolution.

It is possible that the reproductive strategy of the short-beaked echidna is related to seasonal changes in fat deposition and energy availability, regulated by seasonal changes in endocrine function. We predicted that circulating leptin levels would be directly proportional to adiposity during most of the year, but that a change in this relationship would occur during the pre-breeding season to allow increased fat deposition. To test this hypothesis, we made use of a captive colony of echidnas to describe and quantify changes in fat distribution and the adipostatic hormone leptin. First we assessed seasonal changes in circulating leptin levels, body mass and adiposity for three male and three female adult echidnas maintained on a standard diet. Second, we explored the relationship between circulating leptin levels and increased caloric intake for an additional five adult female echidnas that were provided with supplemented nutrition. Third we visualised fat distribution in male and female adult echidnas using magnetic resonance imaging (MRI) before and after the breeding season, to determine where fat is deposited in this species. For echidnas maintained on the standard diet, there were no seasonal changes in body mass, body fat or plasma leptin levels. However, female echidnas provided with supplemented nutrition had significantly elevated plasma leptin levels during the breeding season, compared to the pre-and post- breeding periods. MRI showed substantial subcutaneous fat depots extending dorso-laterally from the base of the skull to the base of the tail, in both sexes. Pre-breeding season, both sexes had considerable fat deposition in the pelvic/rump region, whilst the female echidna accumulated most fat in the abdominal region. This study shows that male and female echidnas accumulate body fat in the pelvic/rump and the abdominal regions, respectively and that circulating leptin may promote fattening in female echidnas during the breeding season by means of leptin resistance. However, further research is required to evaluate the precise relationship between seasonal changes in leptin and adiposity.

Abstract Independently acquired envelope (env) genes from endogenous retroviruses have contributed to the placental trophoblast cell–cell fusion in therian mammals. Egg-laying mammals (monotremes) are an important sister clade for understanding mammalian placental evolution, but the env genes in their genomes have yet to be investigated. Here, env-derived open reading frames (env-ORFs) encoding more than 400 amino acid lengths were searched in the genomes of two monotremes: platypus and echidna. Only two env-ORFs were present in the platypus genome, whereas 121 env-ORFs were found in the echidna genome. The echidna env-ORFs were phylogenetically classified into seven groups named env-Tac1 to -Tac7. Among them, the env-Tac1 group contained only a single gene, and its amino acid sequence showed high similarity to those of the RD114/simian type D retroviruses. Using the pseudotyped virus assay, we demonstrated that the Env-Tac1 protein utilizes echidna sodium-dependent neutral amino acid transporter type 1 and 2 (ASCT1 and ASCT2) as entry receptors. Moreover, the Env-Tac1 protein caused cell–cell fusion in human 293T cells depending on the expression of ASCT1 and ASCT2. These results illustrate that fusogenic env genes are not restricted to placental mammals, providing insights into the evolution of retroviral genes and the placenta.

The function of the skin as a barrier against the environment depends on the differentiation of epidermal keratinocytes into highly resilient corneocytes that form the outermost skin layer. Many genes encoding structural components of corneocytes are clustered in the epidermal differentiation complex (EDC), which has been described in placental and marsupial mammals as well as non-mammalian tetrapods. Here, we analyzed the genomes of the platypus ( Ornithorhynchus anatinus ) and the echidna ( Tachyglossus aculeatus ) to determine the gene composition of the EDC in the basal clade of mammals, the monotremes. We report that mammal-specific subfamilies of EDC genes encoding small proline-rich proteins (SPRRs) and late cornified envelope proteins as well as single-copy EDC genes such as involucrin are conserved in monotremes, suggesting that they have originated in stem mammals. Monotremes have at least one gene homologous to the group of filaggrin ( FLG ), FLG2 and hornerin ( HRNR ) in placental mammals, but no clear one-to-one pairwise ortholog of either FLG , FLG2 or HRNR . Caspase-14, a keratinocyte differentiation-associated protease implicated in the processing of filaggrin, is encoded by at least 3 gene copies in the echidna. Our results reveal evolutionarily conserved and clade-specific features of the genetic regulation of epidermal differentiation in monotremes.

Background Egg-laying mammals (monotremes) evolved multiple sex chromosomes independently of therian mammals and lack the sex-determining gene SRY . The Y-localized anti-Müllerian hormone gene ( AMHY ) is the candidate sex-determination gene in monotremes. Here, we describe the evolution of monotreme AMHX and AMHY gametologues and for the first time, investigate their expression during gonad sexual differentiation in a monotreme. Results Monotreme AMHX and AMHY have significant sequence divergence at the promoter, gene, and protein level, likely following an original allele inversion in the early stages of monotreme sex chromosome differentiation but retaining the conserved features of TGF-β molecules. We show that the expression of sexual differentiation genes in the echidna fetal gonad, including DMRT1 and SOX9 , is significantly different from that of therian mammals. Importantly, AMHY is expressed exclusively in the male gonad during sexual differentiation consistent with a role as the primary sex-determination gene whereas AMHX is expressed in both sexes. Experimental ectopic expression of platypus AMHX or AMHY in the chicken embryo did not masculinize the female urogenital system, as does chicken AMH, a possible result of mammalian-specific changes to AMH proteins preventing function in the chicken. Conclusions Our results provide insight into the early steps of monotreme sex chromosome evolution and sex determination with developmental expression data strongly supporting AMHY as the primary male sex-determination gene of platypus and echidna.

Torpor and reproduction in mammals and birds are widely viewed as mutually exclusive processes because of opposing energetic and hormonal demands. However, the reported number of heterothermic species that express torpor during reproduction is ever increasing, to some extent because of recent work on free-ranging animals. We summarize current knowledge about those heterothermic mammals that do not express torpor during reproduction and, in contrast, examine those heterothermic birds and mammals that do use torpor during reproduction. Incompatibility between torpor and reproduction occurs mainly in high-latitude sciurid and cricetid rodents, which live in strongly seasonal, but predictably productive habitats in summer. In contrast, torpor during incubation, brooding, pregnancy, or lactation occurs in nightjars, hummingbirds, echidnas, several marsupials, tenrecs, hedgehogs, bats, carnivores, mouse lemurs, and dormice. Animals that enter torpor during reproduction often are found in unpredictable habitats, in which seasonal availability of food can be cut short by changes in weather, or are species that reproduce fully or partially during winter. Moreover, animals that use torpor during the reproductive period have relatively low reproductive costs, are largely insectivorous, carnivorous, or nectarivorous, and thus rely on food that can be unpredictable or strongly seasonal. These species with relatively unpredictable food supplies must gain an advantage by using torpor during reproduction because the main cost is an extension of the reproductive period; the benefit is increased survival of parent and offspring, and thus fitness.

1. The effects of mammalian ecosystem engineers on soil microbial communities and ecosystem functions in terrestrial ecosystems are poorly known. Disturbance from livestock has been widely reported to reduce soil function, but disturbance by animals that forage in the soil may partially offset these negative effects of livestock, directly and/or indirectly by shifting the composition and diversity of soil microbial communities. Understanding the role of disturbance from livestock and ecosystem engineers in driving soil microbes and functions is essential for formulating sustainable ecosystem management and conservation policies. 2. We compared soil bacterial community composition and enzyme concentrations within four microsites: foraging pits of two vertebrates, the indigenous short-beaked echidna (Tachyglossus aculeatus) and the exotic European rabbit (Oryctolagus cuniculus), and surface and subsurface soils along a gradient in grazing-induced disturbance in an arid woodland. 3. Microbial community composition varied little across the disturbance gradient, but there were substantial differences among the four microsites. Echidna pits supported a lower relative abundance of Acidobacteria and Cyanobacteria, but a higher relative abundance of Proteobacteria than rabbit pits and surface microsites. Moreover, these microsite differences varied with disturbance. Rabbit pits had a similar profile to the subsoil or the surface soils under moderate and high, but not low disturbance. 4. Overall, echidna foraging pits had the greatest positive effect on function, assessed as mean enzyme concentrations, but rabbits had the least. The positive effects of echidna foraging on function were indirectly driven via microbial community composition. In particular, increasing activity was positively associated with increasing relative abundance of Proteobacteria, but decreasing Acidobacteria. 5. Our study suggests that soil disturbance by animals may offset, to some degree, the oft-reported negative effects of grazing-induced disturbance on soil function. Further, our results suggest that most of this effect will be derived from echidnas, with little positive effects due to rabbits. Activities that enhance the habitat for echidnas or reduce rabbit populations are likely to have a positive effect on soil function in these systems.

Echidnas are egg‐laying mammals found across Australia, and in Tasmania they hibernate, resulting in a most unusual mating system: males enter hibernation in late summer–early autumn and arouse in late autumn–early winter to mate, although females are still hibernating. Groups of males compete for matings and both males and females mate with multiple partners. Females that mate early return to hibernation even when pregnant, and males continue to mate with pregnant females. We asked to what extent can the bizarre combination of behavioural and physiological features that characterize reproduction of Tasmanian echidnas be attributed to their phylogeny, and how much is a consequence of their ecology? To understand the interaction between energetics and the echidna mating system in determining the timing of echidna hibernation, we analysed data from an 18‐year study of a wild population of Tasmanian echidnas (Tachyglossus aculeatus setosus) Males in best condition arouse earliest and seek out suitable females, and females that mate early in the mating season re‐enter hibernation while pregnant. Competition between males drives early mating and while mating with males in the best condition could be advantageous for females and their young, egg‐laying in winter is potentially disadvantageous, and post‐mating hibernation by females is a means of delaying hatching of young until environmental conditions are more favourable. This post‐mating hibernation by females is usually disrupted by males which mate with them although they are already pregnant. Comparisons with other echidna populations suggest that a decreased activity period due to hibernation has not increased male–male competition. Similar competition between groups of males for access to females is seen in chlamyphorid armadillos, which occupy a similar ecological niche to echidnas. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.

The regressive evolution of independent lineages often results in convergent phenotypes. Several teleost groups display secondary loss of the stomach, and four gastric genes, atp4a , atp4b , pgc , and pga2 have been co-deleted in agastric (stomachless) fish. Analyses of genotypic convergence among agastric fishes showed that four genes, slc26a9 , kcne2 , cldn18a , and vsig1 , were co-deleted or pseudogenized in most agastric fishes of the four major groups. kcne2 and vsig1 were also deleted or pseudogenized in the agastric monotreme echidna and platypus, respectively. In the stomachs of sticklebacks, these genes are expressed in gastric gland cells or surface epithelial cells. An ohnolog of cldn18 was retained in some agastric teleosts but exhibited an increased non-synonymous substitution when compared with gastric species. These results revealed novel convergent gene losses at multiple loci among the four major groups of agastric fish, as well as a single gene loss in the echidna and platypus. Several teleost groups display secondary loss of the stomach. Analyses of genotypic convergence among agastric fishes showed that four genes, slc26a9 , kcne2 , cldn18a , and vsig1 , are co-deleted or pseudogenized in most agastric fishes.