Evolution of rat crania in an urban environment

Blog written by Emily Puckett & Liz Carlen. Read the full paper here.

Observations of numerous animal populations have documented morphometric changes in response to urbanization.  Examples abound including: urban populations of anole lizards have longer limbs and more toe lamellae that aid in moving on artificial substrates, urban fish have more streamlined body shapes for swimming in faster flowing streams, and urban damselflies have greater flight endurance.  Additionally, there are numerous examples of changes in skull shape in response to urbanization.  There’s an intuitiveness to these results; artificial lighting means eyes could be smaller and still see at night, complex landscapes could increase brain size/cognition as animals explore novel environments, and altered food resources could shift dentition or beak shapes.  And yet there is a counter argument that urban environments are highly stable in resources, temperature, and landscape, lacking the disturbance of natural environments.  For example, urban environments have stable sources of anthropogenic food waste year-round.

One hypothesis is that populations living in environments that transition from rural to urban show increases in braincase and brain size over time due to plasticity, that then decreases following acclimatization (blue line in figure).  Yet, a second pattern could emerge where the rate of shape change slows precipitously following exposure to the new environment, and thus shape is either maintained through time or changes more slowly (purple lines in figure). Thus, for any population, has urbanization affected cranial shape to increase survival; and if so, how?

We were part of a team investigating the evolution of urban brown rats (Rattus norvegicus) in Manhattan, NY, USA.  We trapped, euthanized and prepared 44 rats as museum specimens.  Fortunately, a series of brown rats were also collected between 1891-1895 allowing us to compare cranial and mandible shape over time using geometric morphometrics.  We hypothesized that due to increasing selection pressures from urbanization, the braincase would increase (in response to exploration of novel environments), the nose would shorten (in response to a warmer urban environment), and the tooth row would shorten (in response to higher quality and softer anthropogenic food).

We observed morphometric differences in both the crania and mandibles between the two sampling times (1890s and 2010s).  Crania of the contemporary samples (2010s) differed from the historic samples (1890s) with a slightly shallower hindbrain case, longer nose, and shorter tooth row.  Our hypothesis about an increasing brain size over time was not supported by our data, although we did observe variation in the hindbrain case related to allometry.  Our hypothesis regarding nose length was in the opposite direction to that we predicted.  We thought that heat island effects would select for larger nasal cavities able to better dissipate heat.  Our hypothesis of a shorter molar tooth row was supported.  This is consistent with rural-urban gradient studies that have shown that as rodents encounter either higher quality and/or softer diets, tooth row length decreases.

We also used the EvolQG package in R to test if the observed shape changes were consistent with directional selection, or the null model of genetic drift.  Our analysis suggested directional selection for shape change of the crania, and drift on the mandible.  Beyond a dietary shift towards softer and more processed foods, our data do not suggest specific aspects of urbanization that may explain the change in shape over time.  We recognize that urbanization creates multiple novel selection pressures, which likely acted jointly on this population of rats.

The prescient question now is, what’s next?  Specifically, will one or more aspects of skull shape shift towards the 1890s shape suggesting a plastic change?  Or will the morphometric changes be retained in the population (or continue on a directional trend)?  And if the latter, how long has this population maintained the current variation for shape?  Due to the presence of only two time points in our temporal sample, we were unable to distinguish between the trajectories for brown rats in Manhattan.

We want to end by acknowledging the collaborators we never knew, the AMNH scientists who collected and prepared the 1890s series of brown rats.  We would not have a study without their work.  Our paper highlights how museum collections benefit from collecting local species. No one knows what questions scientists will want to ask or be able to answer in the future, and by documenting the wildlife that is currently occurring in cities around the world we will be better able to understand how urbanization influences the evolution of species.

Rock hyraxes in the city; the bi-directional effects of cultural norms on urban wildlife

Blog written by Noam Ben-Moshe and Takuya Iwamura . Read the full paper here.

At first sight, it looked like a junkyard in the middle of the neighbourhood, but as we approached, we noticed it was actually a kindergarten. In the Hassidic neighbourhood of Neve Ya’akov of north Jerusalem, several mobile structures stood surrounded by messy piles of children’s chairs, broken swings, and construction waste. The makeshift playground was covered with small, round feces and the acrid smell of urine was strong.

As we entered the compound, the doors burst open and the children came running out, eager to enjoy every second of their break time. There were no proper toys to play with, but everyone seemed to be aiming for a familiar attraction. They began to throw stones at the waste piles. Suddenly, as though responding to the children’s demands upon them, a large group of rock hyraxes appeared from the crevices.

Some of the children started chasing them in circles until the animals fled under one of the trailers while other hyraxes climbed the walls of the structures and began jumping from roof to roof to the sound of the children’s wailing. Another group of hyraxes gathered in the corner of the yard and ate flakes of an Israeli snack called Bamba that a number of children threw at them. The manager of the place approached us to ask if we were from the municipality and if we had come to pick up the animals that he said had “taken over” the garden. Whilst we were talking, we noticed that the manager, on an exposed area of his arm, had a large, muggy lesion. We were familiar with this type of skin infection. It looked like Leishmaniasis, a zoonotic skin disease transferred to humans by a sandfly sting. Rock hyraxes, as found only in recent years, are reservoir hosts of the pathogen causing the disease.

Artificial rock mounds, a by-product of the common building practices in Jerusalem, encircle the new neighbourhoods and create great shelters for wild rock hyraxes next to rich foraging grounds in the city parks.

We were visiting this community as part of our field study work, to understand the drivers that brought these wild animals from their native habitats in secluded canyons in the Judean desert to establish colonies in a core urban area up on the mountains. We also tried to understand why the animals had proliferated in one particular neighbourhood but not in another. Following the hyraxes’ expansion route, we based our research on habitat surveys and hyrax observations in the peripheral areas outside Jerusalem as well as inside the city.

The natural distribution of the rock hyraxes, as their names suggest, is associated with rock piles where they find shelter from predators and adverse weather conditions. While urban sprawl usually causes the extinction or relocation of local wildlife species, observation records show that hyraxes moved towards the city as it expanded.

Urban building practices and heavy machinery, used for the excavation and laying of new roadways, have pushed discarded piles of the rocks down the mountains and into valleys below. This debris have built up over time, and have become urban simulations of the hyrax habitats enveloping the new neighborhoods. We found that these artificial rock piles are great shelters for the hyraxes and they come with the added benefits of providing access to human waste and rich foraging grounds in the adjacent city parks. This combination of shelter and food security has created a fertile environment, which is promoting extremely dense population of hyraxes, while new unoccupied shelters become scarce.

Our findings suggest that these processes have caused a “spill-over” into the urban areas where these new urban invaders are demonstrating highly adaptive skills while taking advantage of the human cultural norms.

Hyraxes demonstrate little fear of humans in the urban parks of north Jerusalem.

Remarkably, we found that in the poorer and more religious areas of the urban environment, there were plenty of sites offering shelter and food in the middle of the urban area. The reason being was that in the poor areas, there seemed to be lack of municipal care, which you would find in more affluent areas. Moreover, in the poor areas there was a lack of awareness around environmental waste management by the local residents, which was demonstrated by the disposal and accumulation of dry waste in open grounds, as well as illegal building with mobile structures that are elevated from the ground; both make complex shelters that are an urban alternative to natural rock piles. To compliment this, a religious prohibition of dumping valuable food means that food items are left in open spaces. Consequently, the rock hyraxes are more common in the poor religious areas, and were not found in high-maintained areas.

In regard to the kindergarten manager we met earlier, and consistent with our research, we found that the largest outbreak of leishmaniasis in the city was next to the highest concentrations of hyrax colonies.

The story of the rock hyrax in Jerusalem could have been a great example for reconciliation ecology, a win-win situation in which a wildlife species flourishes amidst humans, while humans can enjoy observing these playful diurnal animals by their houses. Unfortunately, it is not so, as the animals dispersal is related to a spread of a disease in highly populated areas.

However, since the process is human-driven, we have the means to control it, instead of it controlling us. If we are smarter and adopt a more informed rural-urban strategy, we can manage the spread of the hyraxes in human settlements.

From our studies, observations and investigations, we feel that the following measures should be considered;

  • Enforcement of regulations on building practices, to prevent the common practice of pushing over rock debris from construction sites outside the city and improper placement of mobile structures in the urban areas.
  • Municipal investment in the maintenance of open grounds and a robust waste removal service.
  • Raise awareness and educate human communities about sanitation and how traditions, although well intentioned, may be having a negative effect on their health and well-being.

In these strange times when most of the world’s urban population is under the risk of another zoonotic disease, the last measure may be of the highest priority. 

On the use of microbiome science for captive breeding management practices in species conservation

Blog post by Pauline van Leeuwen and Jasmine Veitch. Read the full paper here. Featured image of Peromyscus sp. by H. Wilson.

A tiny white-footed mouse covertly scours the woodland forest, looking for a tasty snack. As she makes her way through the forest, the tall maple hardwood stands of the Rouge Valley (Greater Toronto Area) stretch far above her towards the open sky. The moonlight peers through the branches, reflecting off of this small creature’s white coat that extends from the mouse’s bottom lip, across her belly, towards petite foot pads. Huge black eyes blink out from her furry face, her keen sense of hearing and smell on high alert as she surveys her landscape. These features make her remarkably efficient as a nocturnal animal. However, as she continues her journey across the forest floor she is not alone.

Invisible to the naked eye, billions of microbes are moving throughout the forest as well. Some of these microbes are simply spectators to the agile mouse, while others are tiny hitchhikers along for the ride. And what a small world! Viruses, protozoa, fungi, archea, bacteria, all forming communities within an animal, called the microbiota. However, with all these passengers, what can we consider an animal? Is it only the host, or all its microbes as well? With advances in microbiome science, old theoretical questions have been brought back to light from another perspective.

In fact, just as large-scale ecosystems provide services to humankind, the microbiota contribute many vital services for its host. These services, or functions, are beneficial for the host and can be essential for survival (McKenney et al., 2018). In the case of the gut microbiota, it plays a substantial role in breaking down food so the host’s body can absorb and digest it. However, that’s not the only role these microbes play – they also support the body’s resistance towards invasive pathogens through direct competition and modulation of the immune system.

Peromyscus sp. by N. Hrynko

So animals are composed of both animal and microbial cells – but where do these microbes come from? We know that there are two types of microbial transmission. The first one is vertical, where a mother passes on her microbiota to her offspring, mainly during vaginal childbirth for mammals. The second type of transmission is horizontal, where microbes can be acquired throughout an individual’s life; such as from the external environment, social interactions, and diet, to name a few.

We used to think that all microbes were equally distributed across the globe but endemicity and biogeography can influence their dispersal. Some microbes are unique to specific body systems and hosts. Like Darwin’s finches in the Galápagos Islands, each host can represent an island with specific finches (or in this case microbes). Local extinctions of microbes can lead to modification of the services they provide for the host, which can have implications for a host’s survival. A good example is humans. Research on the gut microbiome in humans has already given us a sense that the transition from hunter‐gatherer and nomad societies to farming, sedentary, and then urban lifestyles has altered which microbes hang out in our gut. Especially in Western diets, the lack of fibrous foods and increased consumption of processed foods has resulted in reduction of gut bacteria diversity. Loss of these microbes has been implicated in diseases linked to impaired immune responses (asthma, allergies) and metabolic disorders (obesity, type 2 diabetes; Blaser & Falkow, 2009).

However, this phenomenon also applies to other animals and it can become critical when we consider those on the brink of extinction. Many endangered species are under our care and depend on human intervention for their survival. One tool that we possess to help these vulnerable animal populations is captive breeding programs. Offspring are raised in facilities and then released into the wild to prevent populations from collapsing in their natural habitats. Keeping animals in captivity can be somewhat similar to converting to a human westernized lifestyle, but on a much smaller time scale. Since microbes can be acquired through their external environment, captivity can change microbial communities of a host through standardized diets, reduction in natural and seasonal habitat features, and veterinary care.

Research to date shows that the transition from captivity to the wild leads to changes in the microbiome. Captive animals tend to have less diverse microbes and lower abundance, but not in all cases. If animals with distinct food strategies or gut physiology react differently to captivity, it is important to look at these microbiological processes from a wide variety of animals.

Simulating a captive breeding with white-footed mice by P. van Leeuwen

In our study, we investigated how the microbiome of a generalist and omnivorous rodent, the white-footed mouse, varies according to diet change in captivity and upon relocation to its natural habitat. The goal was to determine if a captive version of a wild diet, with non-processed foods, would foster higher gut microbial diversity compared to dry standardized pellets, once the mice where relocated in their natural habitat. Thus, this experiment simulated the effects of a captive breeding program on the animal’s microbes. We discovered that captive animals under the wild non-processed diet had more bacteria in common with their wild counterparts. Moreover, these bacteria might be beneficial for the mice in terms of food degradation and assimilation.

These results are encouraging and show that management practices in captive breeding programs can be modified to limit the impacts of captivity on an animal’s microbiome and potentially its survival back into the wild. However, questions remain on the actual survival and reproductive success of these relocated mice. More work is needed to look at the specific function of each microbe to its host and to monitor relocated animals in the wild to investigate if changes in management practices have long-term effects. Moreover, similar research into different species with other feeding strategies is highly encouraged. For example, our future work will investigate how herbivorous rodents might experience different changes in their microbiome, like the endangered Vancouver Island Marmot. Thinking back to the tiny white-footed mouse cruising about the woodland forest, one might think twice about what defines the boundaries of an individual. Does she alone make up an animal, or do all her invisible passengers make her what she is?

Back to wild by Pauline van Leeuwen

Blaser, M. J., & Falkow, S. (2009). What are the consequences of the disappearing human microbiota? Nature Reviews Microbiology, 7(12), 887–894. doi: 10.1038/nrmicro2245

McKenney, E. A., Koelle, K., Dunn, R. R., & Yoder, A. D. (2018). The ecosystem services of animal microbiomes. Molecular Ecology, 27(February), 2164–2172. doi: 10.1111/mec.14532

Competition from ants may drive spatial patterns of songbirds in the Eastern Himalaya

Blog written by Jordan Greer. Read the full article here

The foothills of the Eastern Himalaya are a warm, lush ecosystem with trees that reach over 20 meters in height, and a network of branches woven throughout the canopy. At 1500 meters up the mountain, the landscape transforms into cool cloud forest, with cascades of falling moss and an almost ever-present mist. And despite the immense diversity of plants and animals in the cloud forest, ants are almost non-existent.

Ants are found throughout the world, even in harsh environments like the Arctic Circle. Surprisingly, however, most ant species are unable to establish in the mid elevations of the Eastern Himalaya. Some theories suggest that the consistent cold and wet climate of cloud forests prevent ants from establishing their colonies. In contrast, within the foothills ants are in abundance. The dominant ant species at low elevation is the weaver ant (Oecophylla smaragdina)– an insectivorous species that “weaves” leaves together to create nests in tree branches. Highly aggressive, weaver ants guard the trees in which they dwell, and forage for food both arboreally and on the forest floor.  As these common predators are not present above low-elevation, researchers sought to understand how their presence (or lack of it) may impact the surrounding ecological community.

Songbirds are present at both low and mid-elevations, though within the cloud forests the number of species is roughly double. Guided by Dr. Trevor Price, an expert on Himalayan bird biodiversity and Dr. Corrie Moreau, one of the world’s leading ant experts, first author Supriya wished to investigate whether there could be a link between the burst of songbird species and the lack of weaver ants within the cloud forest region. If songbirds and weaver ants foraged for the same insects, the absence of weaver ants could potentially open niche space for more species of insectivorous songbirds to occupy. This could also explain why in the foothills, where weaver ants are common, there are significantly less species of songbirds—by ants acting as resource competitors, they may influence spatial patterns of songbird diversity.

The fossil record could lend support to this idea. Weaver ant species used to be found globally, including Europe. Interestingly, around the same time weaver ants disappeared from the European fossil record, scientists recorded the earliest songbird fossil in Germany. Though speculative, if both animals occupied the same niche, this could act as an early example of how weaver ant presence could influence the spatial patterns and even diversification of songbird species.

Weaver ants carrying insects into their nest in Chapramari Wildlife Sanctuary, India. (Photo: K. Supriya)

To test whether weaver ants could act as a strong resource competitor to songbirds in the Eastern Himalaya, Supriya first needed to establish that both seek out the same food sources. The researchers extracted animal DNA from songbird fecal matter at both low and mid elevation habitat, and compared that to DNA extracted from weaver ant food removed from their colony. The results demonstrated a significant overlap in the diets of weaver ant and songbirds at both elevations— each with a strong appetite for Coleoptera (beetles) and Lepidoptera (butterflies and moths) in particular.

But even though their diets overlap, that doesn’t necessarily mean weaver ants are so voracious in appetite that they exclude birds from occupying habitats by limiting food. To better address this, Supriya asked whether weaver ants significantly depleted the number of arthropods from the trees in which they lived. In the forests near the lowland village of Panijhora, where much of the field research was carried out, she and her field team took on the grueling task of pairing equally sized trees of the same species with and without weaver ant nests. Then they assessed both the insect abundance and the amount of leaf damage present. They found that the abundance of Lepidoptera and Coleoptera was nearly twice as high in trees without weaver ants.

To make sure this finding wasn’t just the result of ant preference for trees with less insects, they followed up with an ant exclusion experiment. Here, the researchers removed all weaver ant nests from several trees and applied a band of TanglefootTM around the trunk to prevent ants from recolonizing. Measures of arthropod abundance were taken before and one month after weaver ant removal. This allowed investigators to tease out if non-ant arthropods could “bounce back” to greater abundance once ants were removed. On average, after one-month trees with ants removed showed 3 times increase in their insect abundance.

Supriya and her 2016 field team (Amir Chhetri, Jobin Varughese, Priyanka Das, Vinod Sankar) sampling arthropods at a tree (Photo: Corrie Moreau)

Taken together, these results suggest that the absence of weaver ants has a positive impact on arthropod abundance. As such, the absence of ants at mid-elevation may contribute to the high non-ant arthropod density within the cloud forest region. In addition, diet overlap analysis shows birds and ants likely compete for arthropod prey at low elevations in the Eastern Himalaya. The lack of competition between ants and songbirds at mid elevation could be one potential driver for the witnessed increase in insectivorous songbird diversity.

A major takeaway from this study is that it is limiting to only look at competition between two closely related species, as is often done. We must also consider the broader communities and guilds in which species take part—these relationships can be as important or more to ecosystem structure. Further, as community ecology research progresses, we need to better address communities that exist across or over regional or environmental climatic gradients, especially in the face of climate change. Could climate change reshape the weaver ants’ distribution to move into cloud forest? And if so, would they displace the resident songbird species? Many questions are left to be answered, but this study acts as an initial step towards tackling questions about community structure within the Himalayas.

Understanding Phylogeographic Histories in an Understudied Region: Historical DNA Coming to the Rescue

Blog written by Haw Chuan Lim. Featured image by Paul van Els. Read the full paper here.

Questions such as why tropical regions are so rich in biological diversity, and how historical and ecological factors shaped the origin and distribution of tropical species have intrigued scientists for generations. Thankfully, exciting improvements in molecular genetics and analytical tools over the last few decades have allowed us to progressively peel back the layers. For example, we now the know the roles large Amazonian rivers and the Andes play in terms of initiating and maintaining species divergence in South America (Naka & Brumfield, 2018).

Image by Paul van Els

Interest in the biogeography and evolutionary history of Southeast Asian plants and animals dates back to Alfred Russel Wallace and earlier. Although researchers have made great strides, especially in the last decade or so (Sheldon, Lim, & Moyle, 2015), it remains a challenge to conduct phylogeographic studies in Southeast Asia. Many areas in Southeast Asia, which is made up of biogeographic subregions such as Indochina, Sundaland and the Philippines, have not been systematically sampled because of logistic and administrative challenges. Further, the region is “feature-packed” when it comes to the diversity of biogeographic processes. In a relatively small area, Southeast Asia contains everything from oceanic archipelagos to continental areas dissected by rivers, mountain ranges and diverse habitat types. Thus, dense sampling is required to produce comprehensive understanding of the historical and geographic drivers of population divergence and speciation.

Grey-throated babbler by Dibyedu Ash, CC3.0

Because of these challenges, past studies have largely taken a piecemeal approach to phylogeographic studies. For example, work in Borneo showed that drier habitats that appeared during past glacial maxima likely caused lowland rainforest species to split into eastern and western forms (Lim et al., 2017). Some studies have shown that the Isthmus of Kra, the narrow land bridge in southern Thailand that connects Sundaland and Indochina also separates sister species or closely related populations (Manawatthana, Laosinchai, Onparn, Brockelman, & Round, 2017).

Black-headed Bubul, by Doug Janson CC3.0

In this study, we used techniques that allow us to sequence thousands of genetic markers using DNA extracted from old (from late 1800’s onwards) museum study skins to investigate phylogeography of five species of rainforest-associated passerine birds that co-occur across much of Indochina and Sundaland. While technically challenging, this approach let us achieve comprehensive and relatively even geographic sampling for each of the five species. The massive amount of genetic data generated enable high-resolution studies of population structure and historical demographic processes, thus providing insights that were previously unavailable.

Large Niltava by Ajit Hota, CC4.0

We discovered that the phylogeographic patterns of the study species largely agree with their ecological characteristics. The Black-headed Bulbul, a frugivore/insectivore species that often uses forest edges, shows little population genetic structure across the entire Sundaland and parts of western Indochina. In contrast, the Little Spiderhunter and Asian Fairy-Bluebird possess highly distinct populations in peripheral Sunda islands (Java and/or Palawan) and India. This is probably due to their intermediate dispersal abilities, which allowed them to colonize new areas, and then remain largely isolated subsequently. Such dispersal events could occur during periods of low global sea-level, which exposed land bridges. A north-south population break across the Isthmus of Kra is shared only by the two species (Gray-throated Babbler and Large Niltava) that live in hill/submontane habitats. This suggests that the low elevation of the Isthmus of Kra had contributed to population splitting or the maintenance of population separation in the two species.

Little Spiderhunter by Lip Yee Kap, CC2.0

Interestingly, the Black-headed Bulbul and Gray-throated Babbler, two species with different ecological characteristics, show an east-west break in Indochina. This break is associated with the central mountain (Tennasserim) range of Indochina or the dry Irrawaddy plains of central Myanmar. Without the use of DNA from old museum skins, the discovery of genetic breaks in this region will be very difficult because it has rarely been visited by museum scientists in recent years. In each of the five species, the deepest split dates back to 1-1.5 million years ago. This coincidence in timing suggests that region-wide environmental upheavals –likely those associated with glacial cycles – played important roles in splitting populations and structuring genetic diversity.

Asian Fairy-Bluebird by Tony Castro, CC4.0

With the accelerating loss of forest habitats across Southeast Asia, it is imperative that we improve our understanding of what makes up significant evolutionary units within species, and what historical, environmental and geographic factors caused these units to form and persist. Advances in phylogeographic studies in Southeast Asia, a biologically rich region composed of multiple biodiversity hotspots, will depend on broad geographic sampling and the use of increasingly sophisticated molecular genetics and analytical techniques.

Picture by Haw Chuan Lim

Lim, H. C., Gawin, D. F., Shakya, S. B., Harvey, M. G., Rahman, M. A., & Sheldon, F. H. (2017). Sundaland’s east–west rain forest population structure: variable manifestations in four polytypic bird species examined using RAD-Seq and plumage analyses. Journal of Biogeography, 44(10), 2259-2271. doi:10.1111/jbi.13031

Manawatthana, S., Laosinchai, P., Onparn, N., Brockelman, W. Y., & Round, P. D. (2017). Phylogeography of bulbuls in the genus Iole (Aves: Pycnonotidae). Biological Journal of the Linnean Society, 120(4), 931-944.

Naka, L. N., & Brumfield, R. T. (2018). The dual role of Amazonian rivers in the generation and maintenance of avian diversity. Science Advances, 4(8), eaar8575. doi:10.1126/sciadv.aar8575

Sheldon, F., Lim, H. C., & Moyle, R. (2015). Return to the Malay Archipelago: the biogeography of Sundaic rainforest birds. Journal of Ornithology, 156 (Supplemental 1), 91-113.

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