Diet of the introduced Gough Moorhen Gallinula comeri on Tristan da Cunha

Gough Moorhens Gallinula comeri were introduced to Tristan da Cunha in the 1950s, and are now numerous in lowland habitat, filling the ecological niche of the extinct Tristan Moorhen G. nesiotis. On their native Gough Island, moorhens have a varied diet, ranging from vegetation and fruits to scavenging and even predatory behaviour. Here, we examined the stomach contents of four birds on Tristan da Cunha to provide insight into their diet. Moorhens mostly ate vegetation, but we also recorded spiders (Arthropoda: Aranea), earthworms (Oligochaeta: Lumbricidae), remains of introduced rodents (Mus musculus), and anthropogenic debris. As on Gough Island, moorhens on Tristan have a generalist diet, and the impact of ecosystem restoration (and of the moorhens themselves) should be considered.

Evolution of boldness and exploratory behavior in giant mice from Gough Island

Island populations are hallmarks of extreme phenotypic evolution. Radical changes in resource availability and predation risk accompanying island colonization drive changes in behavior, which Darwin likened to tameness in domesticated animals. Although many examples of animal boldness are found on islands, the heritability of observed behaviors, a requirement for evolution, remains largely unknown. To fill this gap, we profiled anxiety and exploration in island and mainland inbred strains of house mice raised in a common laboratory environment. The island strain was descended from mice on Gough Island, the largest wild house mice on record. Experiments utilizing open environments across two ages showed that Gough Island mice are bolder and more exploratory, even when a shelter is provided. Concurrently, Gough Island mice retain an avoidance response to predator urine. F1 offspring from crosses between these two strains behave more similarly to the mainland strain for most traits, suggesting recessive mutations contributed to behavioral evolution on the island. Our results provide a rare example of novel, inherited behaviors in an island population and demonstrate that behavioral evolution can be specific to different forms of perceived danger. Our discoveries pave the way for a genetic understanding of how island populations evolve unusual behaviors. Significance Organisms on islands are known to behave differently from mainland organisms. An absence of predators and a different set of natural resources are expected to make island organisms less anxious and more exploratory. We raised two groups of house mice, one from Gough Island in the South Atlantic and one from the mainland Eastern USA, in the same laboratory environment to see if behavioral differences between the two groups are heritable. Mice from both groups were placed in novel enclosures that are known to cause anxiety in rodents. We found that mice from the island are bolder and more exploratory in these enclosures but avoid predator odors in the same way as mainland mice. Our results show that boldness and exploration can evolve after island colonization.

A juvenile Tristan albatross (Diomedea dabbenena) on land at the Crozet Islands

Albatrosses and other seabirds are generally highly philopatric, returning to natal colonies when they achieve breeding age. This is not universal, however, and cases of extraordinary vagrancy are rare. The Tristan Albatross (Diomedea dabbenena) breeds on Gough Island in the South Atlantic Ocean, with a small population on Inaccessible Island, Tristan da Cunha, ca 380 km away. In 2015, we observed an adult male albatross in Gonydale, Gough Island, which had been ringed on Ile de la Possession, Crozet Islands in 2009 when it was assumed to be an immature Wandering Albatross (D. exulans). We sequenced 1109 bp of the cytochrome b mitochondrial gene from this bird, and confirmed it to be a Tristan Albatross, meaning its presence on Crozet 6 years previous, and nearly 5000 km away, was a case of prospecting behaviour in a heterospecific colony. Given the challenges in identifying immature Diomedea albatrosses, such dispersal events may be more common than thought previously.

Important marine areas for the conservation of northern rockhopper penguins within the Tristan da Cunha Exclusive Economic Zone

The designation of Marine Protected Areas has become an important approach to conserving marine ecosystems that relies on robust information on the spatial distribution of biodiversity. We used GPS tracking data to identify marine Important Bird and Biodiversity Areas (IBAs) for the Endangered northern rockhopper penguin Eudyptes moseleyi within the Exclusive Economic Zone (EEZ) of Tristan da Cunha in the South Atlantic. Penguins were tracked throughout their breeding season from 3 of the 4 main islands in the Tristan da Cunha group. Foraging trips remained largely within the EEZ, with the exception of those from Gough Island during the incubation stage. We found substantial variability in trip duration and foraging range among breeding stages and islands, consistent use of areas among years and spatial segregation of the areas used by neighbouring islands. For colonies with no or insufficient tracking data, we defined marine IBAs based on the mean maximum foraging range and merged the areas identified to propose IBAs around the Tristan da Cunha archipelago and Gough Island. The 2 proposed marine IBAs encompass 2% of Tristan da Cunha’s EEZ, and are used by all northern rockhopper penguins breeding in the Tristan da Cunha group, representing ~90% of the global population. Currently, one of the main threats to northern rockhopper penguins within the Tristan da Cunha EEZ is marine pollution from shipping, and the risk of this would be reduced by declaring waters within 50 nautical miles of the coast as ‘areas to be avoided’.

Mouse eradication is required to prevent local extinction of an endangered seabird on an oceanic island

Petrels (Procellariidae) are a highly diverse family of seabirds, many of which are globally threatened due to the impact of invasive species on breeding populations. While predation by invasive cats and rats has led to the extinction of petrel populations, the impact of invasive house mice Mus musculus is slower and less well documented. However, mice impact small burrow-nesting species such as MacGillivray’s prion Pachyptila macgillivrayi, a species classified as endangered because it has been extirpated on islands in the Indian Ocean by introduced rodents. We use historic abundance data and demographic monitoring data from 2014 to 2020 to predict the population trajectory of MacGillivray’s prion on Gough Island with and without a mouse eradication using a stochastic integrated population model. Given very low annual breeding success (0.01 fledglings per breeding pair in ‘poor’ years (83%) or 0.38 in ‘good’ years (17%), n = 320 nests over 6 years) mainly due to mouse predation, our model predicted that the population collapsed from ~3.5 million pairs in 1956 to an estimated 175,000 pairs in 2020 despite reasonably high adult survival probability (ϕ = 0.901). Based on these parameters, the population is predicted to decline at a rate of 9% per year over the next 36 years without a mouse eradication, with a 31% probability that by 2057 the MacGillivray’ prion population would become extremely vulnerable to extinction. Our models predict population stability (λ = 1.01) and a lower extinction risk (<10%) if mouse eradication on Gough Island restores annual breeding success to 0.519, which is in line with that of closely-related species on predator-free islands. This study demonstrates the devastating impacts that introduced house mice can have on small burrowing petrels and highlights the urgency to eradicate invasive mammals from oceanic islands.

Genomic Targets of Positive Selection in Giant Mice from Gough Island

A key challenge in understanding how organisms adapt to their environments is to identify the mutations and genes that make it possible. By comparing patterns of sequence variation to neutral predictions across genomes, the targets of positive selection can be located. We applied this logic to house mice that invaded Gough Island, an unusual population that shows phenotypic and ecological hallmarks of selection. We used massively parallel short-read sequencing to survey the genomes of 14 Gough Island mice. We computed a set of summary statistics to capture diverse aspects of variation across these genome sequences, used approximate Bayesian computation to reconstruct a null demographic model, and then applied machine learning to estimate the posterior probability of positive selection in each region of the genome. Using a conservative threshold, 1,463 5kb windows show strong evidence for positive selection in Gough Island mice but not in a mainland reference population of German mice. Disproportionate shares of these selection windows contain genes that harbor derived nonsynonymous mutations with large frequency differences. Over-represented gene ontologies in selection windows emphasize neurological themes. Inspection of genomic regions harboring many selection windows with high posterior probabilities pointed to genes with known effects on exploratory behavior and body size as potential targets. Some genes in these regions contain candidate adaptive variants, including missense mutations and/or putative regulatory mutations. Our results provide a genomic portrait of adaptation to island conditions and position Gough Island mice as a powerful system for understanding the genetic component of natural selection.

Evolution of Boldness and Exploratory Behavior in Giant Mice from Gough Island

Island populations are hallmarks of extreme phenotypic evolution. Radical changes in resource availability and predation risk accompanying island colonization drive changes in behavior, which Darwin likened to tameness in domesticated animals. Although many examples of animal boldness are found on islands, the heritability of observed behaviors, a requirement for evolution, remains largely unknown. To fill this gap, we profiled anxiety and exploration in island and mainland inbred strains of house mice raised in a common laboratory environment. The island strain was descended from mice on Gough Island, the largest wild house mice on record. Experiments utilizing open environments across two ages showed that Gough Island mice are bolder and more exploratory, even when a shelter is provided. Concurrently, Gough Island mice retain an avoidance response to predator urine. F1 offspring from crosses between these two strains behave more similarly to the mainland strain for most traits, suggesting recessive mutations contributed to behavioral evolution on the island. Our results provide a rare example of novel, inherited behaviors in an island population and demonstrate that behavioral evolution can be specific to different forms of perceived danger. Our discoveries pave the way for a genetic understanding of how island populations evolve unusual behaviors.

Giant Island Mice Exhibit Widespread Gene Expression Changes in Key Metabolic Organs

Island populations repeatedly evolve extreme body sizes, but the genomic basis of this pattern remains largely unknown. To understand how organisms on islands evolve gigantism, we compared genome-wide patterns of gene expression in Gough Island mice, the largest wild house mice in the world, and mainland mice from the WSB/EiJ wild-derived inbred strain. We used RNA-seq to quantify differential gene expression in three key metabolic organs: gonadal adipose depot, hypothalamus, and liver. Between 4,000 and 8,800 genes were significantly differentially expressed across the evaluated organs, representing between 20% and 50% of detected transcripts, with 20% or more of differentially expressed transcripts in each organ exhibiting expression fold changes of at least 2×. A minimum of 73 candidate genes for extreme size evolution, including Irs1 and Lrp1, were identified by considering differential expression jointly with other data sets: 1) genomic positions of published quantitative trait loci for body weight and growth rate, 2) whole-genome sequencing of 16 wild-caught Gough Island mice that revealed fixed single-nucleotide differences between the strains, and 3) publicly available tissue-specific regulatory elements. Additionally, patterns of differential expression across three time points in the liver revealed that Arid5b potentially regulates hundreds of genes. Functional enrichment analyses pointed to cell cycling, mitochondrial function, signaling pathways, inflammatory response, and nutrient metabolism as potential causes of weight accumulation in Gough Island mice. Collectively, our results indicate that extensive gene regulatory evolution in metabolic organs accompanied the rapid evolution of gigantism during the short time house mice have inhabited Gough Island.