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Insect herbivores and the drivers of plant speciation

This is a guest post by Christina Baer, a Ph.D. candidate in Ecology, Evolution, and Systematics at the University of Missouri-St. Louis

Fifty-two years ago, two biologists published a huge paper proposing that caterpillars and their food plants evolve in response to each other (Ehrlich and Raven 1964). They presented quite a bit of evidence for this: closely related caterpillars usually eat closely related plants and can tolerate the same defensive chemicals produced by plants. And in the last fifty years, biologists have found many examples of plants changing their chemical defenses in response to insects, or insects evolving new ways to get around plant defenses. But Ehrlich and Raven went one step further and proposed that insect herbivores could cause new plant species to evolve. Unfortunately, they didn’t suggest any step-by-step scenarios for how insects could cause plant speciation, which made it difficult to test the hypothesis. So far, no one has.

Several years ago, the Marquis lab decided that we would try to come up with ways that herbivorous insects could cause new plant species to evolve. To do this, we had to think of ways that insect herbivory could affect different groups within a plant species differently. If the entire species responds the same way, then the species’ characteristics will change, but it will still be one species. So we brainstormed all the different things that could cause individuals to respond differently (location? soil? timing?) and looked for previous research that illustrated each step.

The simplest scenario we developed would apply to plants that use the same chemicals to defend their leaves and attract pollinators. In both cases, simple chemical changes can have dramatic effects on how the animals respond. If some plants evolve new defensive chemicals in response to herbivores, then those same chemicals could attract different pollinators to the flowers. If the original pollinator is not attracted, then the plants with the new chemicals would be reproductively isolated from the rest of the population. Given time, the two groups would separate into different species. To see the other scenarios we came up with, you can check out our new article, “Ode to Ehrlich and Raven or how herbivorous insects might drive plant speciation”.

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Scenarios by which herbivores may coevolve with host plants: a) the reciprocal arms race model, and b) the speciation arms race model. From Marquis et al. 2016.

Writing this article was interesting for me because it was very different from writing up an experiment. With an experiment, you usually start in the middle of the article (the methods and results) and work out to explain why you did the experiment (the introduction) and what it means (the discussion). It’s fairly clear from the beginning what needs to be in the article and how it should be organized. With a conceptual article, it’s much less obvious what needs to be included and it takes even more work than usual to make your ideas clear and organized. I think the article got pulled apart and put together in a completely different order two or three different times while we writing it. At one point, I made a list of each paragraph’s main ideas so that I could arrange them in different orders and see what made the most sense. In the end, it took about as long for us to write the article as it did to come up with the possible scenarios.

Conceptual articles are important for scientists because they rearrange what we know and help us see how we can test ideas in new ways. In this case, we’ve outlined ways of testing for herbivore-driven speciation and pointed out a couple of systems that already have evidence for several steps. We’re hoping that other ecologists will use these ideas to finally test Ehrlich and Raven’s hypothesis. Since most of the scenarios we came up with are complicated, it will be interesting to see how common herbivore-driven speciation is.

Cited papers:

Marquis, R. J., D. Salazar, C. Baer, J. Reinhardt, G. Priest, and K. Barnett. 2016. Ode to Ehrlich and raven or how herbivorous insects might drive plant speciation. Ecology 97:2939-2951.

Ehrlich, P. R. and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.

About the author:

cbaersnapshot

Christina Baer is a PhD candidate in the Marquis Lab at the University of Missouri-St. Louis. Her research interests include plant-insect interactions, natural history, and community ecology, so she’s doing her dissertation research on how tropical caterpillars build shelters to protect themselves from predators and parasitic insects. She wants to be a professor when she grows up.

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The complex ties between Caribbean birds and their bloody parasites

chris-johns-a-culex-mosquito-near-the-eye-of-an-iiwi-bird

The most dramatic picture ever taken of a mosquito biting a bird. Credit: Chris Johns.

Malaria is not a “privilege” of humans. Though mostly known for its devastating impacts on people worldwide, bird populations have also suffered the consequences of infections by this group of parasites. On the early 20th century, the mosquito Culex quinquefasciatus and the parasite Plasmodium relictum were introduced to Hawaii, and by the end of the century had caused the extinction and population decline of several forest birds, in especial the endemic honeycreepers (subfamily Drepanidinae). Since then, the surviving honeycreeper populations have shifted their range to higher and cooler elevations in the Hawaiian archipelago. More recently, some populations have been colonizing lower elevation areas, and microsatellite data suggests that birds from high elevations, which are genetically resistant to malaria, are the ones dispersing back to the original species range. The fact Hawaiian honeycreepers dispersed and re-colonized lower elevation areas was only possible because populations in the cooler and malaria-free environment of higher elevations could grow back in numbers again. Nonetheless, the recovery process of honeycreepers populations is being affected by global warming. Capture-mark-recapture studies with C. quinquefasciatus show that elevated temperatures not only increase the number of infected mosquitoes, but also allow them to disperse to higher elevations. In addition, the main reservoir of avian haemosporidian parasites in Hawaii, the Omahi elepaio (Chasiempis sandwichensis) has also expanded its range towards higher elevations, an event also associated with warmer atmospheric temperatures.

Extinct Hawaiian honeycreepers

Honeycreepers were wiped off by malaria parasites. Extinct Hawaiian honeycreepers at the Bishop Museum, Honolulu, Hawaii. Credit © Frans Lanting/Corbis

The Hawaiian problem with bird malaria, and its recent re-emergence due to climate change, has been serving as a piece of advice for conservation biologists and environmental policy makers in order to avoid that the same happens elsewhere. In birds, malaria is just one of the diseases caused by parasites of the order Haemosporida. The devastating example of Hawaiian birds is perhaps the most well documented effects of Plasmodium sp. parasites on birds populations. However, it’s important to keep in mind that contrary to most of the birds that carry haemosporidian infections worldwide, Hawaiian birds have only been exposed to these parasites more recently, and did not evolve to deal with such a disease. Therefore, the effects of haemosporidian parasites on bird populations that have been dealing with such threat over thousand of years remains poorly investigated. In a recent paper published by our group, we look at the effects of these parasites on bird populations of the West Indies, where hosts have been exposed to parasites over longer periods of time. We looked at the correlation between the frequency of 12 genetically distinct strains of haemosporidian parasites and the abundance of 9 bird populations across 13 islands of the Lesser Antilles.

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We are featured on the cover of the Journal of Biogeography. 

We found a negative relationship between the frequency of parasite strains and the abundance of birds on Lesser Antillean islands. This is groundbreaking because the size of bird populations vary across islands with no obvious ecological explanation. For instance, Lesser Antillean bullfinches are highly abundant in most islands of the archipelago, except for Carriacou in the Grenadines, where these birds are completely absent, despite the suitable ecological conditions for their occurrence. We believe that mortality caused by haemosporidian parasites explain the negative relationships found between pathogen strains and bird abundance. Remarkably, some parasite strains  were positively related to the size of bird populations of species that we never recorded infected with such strains. This suggests that some bird species might benefit from the presence of the parasites if they decrease the population size of competing bird species. This is the classic “the enemy of my enemy is my friend” type of situation.

 

Check out our paper here:

Ricklefs, R.E., Soares, L., Ellis, V.A. & Latta, S.C. (2016) Haemosporidian parasites and avian host population abundance in the Lesser Antilles. Journal of biogeography, 43, 1277–1286.

 

 

 

 

 

Interbreeding, introgression and human evolution: Neanthertal cousins responsible for high altitude adaptation in Tibetans

Tibetans ability to survive in the mountains, where there is 40% less oxygen than at sea level, was donated by Denisovans, which are Neanthertals close relatives. Photo: Lhasa girl, Gaelle Morand, from http://www.planet-mag.com/2011/home/editors/winners-portrait-slideshow/

Tibetans ability to survive in the mountains, where there is 40% less oxygen than at sea level, was donated by Denisovans, which are Neanthertals close relatives. Photo: Lhasa girl, Gaelle Morand, from http://www.planet-mag.com/2011/home/editors/winners-portrait-slideshow/

When I think about Tibetans, what first comes to my mind is the expression of enlightenment in their faces. Maybe because to survive at 14,000 ft of elevation, one needs to have something else, which can be either lots of wisdom or an especial adaptation craved in the genes. In a recent study published in Nature, researches found that this something else that makes Tibetans so successful at colonizing high elevation areas are haplotypes donated by Denisovan hominins through DNA introgression. In a multi-national collaboration, Huerta-Sanchez and colleagues investigated the genetic variation of the gene EPAS1, linked to adaptation to low oxygen levels in high altitudes. When ordinary, non-adapted to high altitude, people are exposed to environments with low concentration of oxygen (hypoxia) the body enters in a compensatory mode. Hemoglobin levels increase, the number of red blood cells boosts, the heart starts to overwork in order to deliver oxygen to all demanding tissues, and finally, blood pressure ramps up to the risk of heart failure and damage to the peripheral circulation. All that doesn’t happen to Tibetans though. Their hemoglobin levels aren’t boosted because of the low oxygen levels, in fact they present similar adaptations of other mammalian species that live in high altitude, such as pigs and antelopes: they have thin walled pulmonary vascular structure, which translates into high gas exchange efficiency, and their blood flows at a higher velocity, meaning that tissues get their oxygen delivered even when the supply is low. All these anatomic and physiologic variations have a direct implication on reproductive success, since women that lack high-altitude adaptation usually have miscarriages due to eclampsia, or fetal heart failure. Given such a tuned phenotype-environment adaptation, one can ask how evolution of altitude adaptation in the Tibetan population took place. In order to disentangle this evolutionary history, Huerta-Sanchez and colleagues put their bet on using SNPs (see bellow) to understand the genetic variability of one gene, EPAS1, a transcription factor associated with the activation of several other genes regulated by oxygen concentration.

Thanks to Denisovans, Tibetans physiology make them well equipped to survive hypoxia. Photo by Lynn Johnson, Nat Geo. http://news.nationalgeographic.com/news/2014/07/140702-genetics-tibetan-denisovan-altitude-science/

Thanks to Denisovans, Tibetans physiology make them well equipped to survive hypoxia. Photo by Lynn Johnson, Nat Geo. http://news.nationalgeographic.com/news/2014/07/140702-genetics-tibetan-denisovan-altitude-science/

Data from Single Nucleotide Polymorphisms (SNPs) analysis have been contributing to understand how altitude adaptation took place. A SNP is a single nucleotide difference in a DNA sequence. These unique changes on the basic building blocks of genes can be associated to several phenotypic differences detectable between populations of the same species. Human arrival in the Tibetan plateau took place in the Last Glacial Maximum, around 25 thousand years ago. Since then, about 1,100 generations of Tibetans have been surviving under high-elevation-related hypoxia – sufficient time for fixation of alleles that confer altitude adaptation. Just looking at the gene EPAS1, Tibetans have shown to present a remarkable SNP diversity when compared to their closely related ethnic group, the Han Chinese, showing the fastest allelic change observed in any human genome to date – how impressive! But, what is the deal with populations that are not highly differentiated, but present considerable difference in the frequency at which specific mutations happen, like Tibetans and Han Chinese for EPAS1 SNPs? Huerta-Sanchez and colleagues hypothesized that the source of variation may come from donor populations. They first tried to understand how so much variation in such a short genomic region evolved, by testing two models of selection that simulate how EPAS1 haplotype diversity evolved: 1) selection under standing variation, assuming that Tibetans already had the beneficial haplotype when they colonized high altitude environments; or 2) selection under de novo mutation, which predicts that beneficial haplotype showed up and was fixed in the population after establishment in high altitudes. Surprisingly, the high haplotype diversity found in Tibetan EPAS1 couldn’t be explained by neither of the models of evolution, which supported the hypothesis that a donor population contributed to the fast EPAS1 diversification: in other words, DNA introgression lead to adaptation.

Haplotype network. Each pie chart is a haplotype, and colors within each pie chart represent the proportions of individuals from all populations that share the same haplotype. The Tibetan haplotypes are closer to the Denisovan than they are from any other modern human population a pattern expected under introgression. Figure and legend adapted from Huerta-Sanchez 2014.

Haplotype network. Each pie chart is a haplotype, and colors within each pie chart represent the proportions of individuals from all populations that share the same haplotype. The Tibetan haplotypes are closer to the Denisovan than they are from any other modern human population a pattern expected under introgression. Figure and legend adapted from Huerta-Sanchez 2014.

Work inside the Denisova cave in Siberia, where Denisovan, Neanthertal and modern humans took shelter from the cold generation after generation, during thousands of years. Photo from: http://ngm.nationalgeographic.com/2013/07/125-missing-human-ancestor/gallery-interactive

Work inside the Denisova cave in Siberia, where Denisovan, Neanthertal and modern humans took shelter from the cold generation after generation, during thousands of years. Photo from: http://ngm.nationalgeographic.com/2013/07/125-missing-human-ancestor/gallery-interactive

By searching for possible donor populations in several genomic databases, the authors found that Tibetans shared several haplotypes with the Denisovan individuals, popularly known as being the Neanthertal cousins. The Denisovan fossil record, even though only composed as whole by two phalanges and two teeth, have rendered amazing insights into hominin evolution since their discovery four years ago, in a cave in Siberia. What Huerta-Sanches and co-authors visualized when they looked at the haplotype networks to understand the relationships between Denisovan, Tibetan and 26 other modern human populations haplotype diversity of the EPAS1 gene was striking: the Tibetan haplotypes are closer to the Denisovan than they are from any other modern human population, a pattern only expected under introgression. Adaptation to high altitude amongst Tibetans may have been facilitated by gene flow from other hominins that may already have been adapted to those environments. This fantastic finding leads to an infinite network of questions: What is the relationship between Tibetans and other human populations adapted to high altitudes, like Basques in the Pyrenees and several ethnic groups in the Andes?  How does the genetic variation of other hypoxia-related genes look like? Are Tibetans good marathonists? How culturally different were Homo sp. populations interbreeding around 30 thousand years ago, did they speak the same language, how different they looked, how long did they interbred for? Should Tibetans thank the DNA donation by creating a new holiday called National Denisovan Day? Well, I suppose this is one of the beauties of science, one question answered, so many more to go.

Thanks to Dr Hughes, who chose this paper to be discussed in the seminar lead by him about Next Generation Sequencing at the Bio Department of the University of Missouri St Louis!

Huerta-Sanchez et al. 2014. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA, Nature 512, 194–197. 

The role of dispersal in Neotropical avian diversity

In a paper published in Nature last month by Brian T. Smith (American Museum of Natural History) and collaborators argue that the strongest predictors of avian speciation in the Amazon are the amount of time a species lineage has endured in the landscape, and how well a bird can move through that landscape. Their results suggest that the dispersal abilities of the birds and how long their lineage has persisted are important drivers of the high biodiversity in the Amazon.

The authors start the introduction by reminding us that we, scientists, usually link the biodiversity of the Neotropics to two major hypotheses:

1) large-scale landscape changes that generate bio-diversification by population fragmentation followed by isolation, and

2) the formation of a geographically structured landscape matrix on which diversification occurred.

The first, commonly known as vicariance, involves reconfigurations of the landscape, such as the separation of continents by plate tectonics, the uplift of mountains or the formation of large rivers. Since the study involves the avian fauna of the Neotropic region, the large-scale events considered by the authors that could drive biodiversity patterns are the Andean mountain uplift, and the formation of the (very large) Amazonian rivers. This first hypothesis is easier to understand: big mountain or rivers separate populations, which can no longer exchange genes and start differentiating from one another to the point where the different sides will have completely separate evolutionary futures.

The second hypothesis involves organisms’ ability to persist in a structured landscape, which does not necessarily need to change. In this case, allopatric speciation would follow dispersal events, and thus, organism-specific abilities to persist and disperse in the landscape are the principal drivers of speciation. Species with lower dispersal abilities have a lower chance of navigating the landscape and, therefore, tend to accumulate higher genetic differentiation between populations. Higher differentiation, in turn, leads to higher speciation rates.

Figure 1 from Smith et al. 2014. Main landscape barriers and data points in the Neotropics.

Figure 1 from Smith et al. 2014. Main landscape barriers and data points in the Neotropics.

To test these two hypotheses, the authors used 2,500 individuals from 27 widespread bird lineages in the Neotropics. To prevent biases of current taxonomic limitations, authors considered lineages instead of species, i. e., they used monophyletic groups as their definition of a lineage instead of going by current taxonomic nomenclature.

They looked at relatively recently diversified lineages that have their distribution interrupted by the Andes, the Isthmus of Panama and large rivers of the Amazon Basin (the Amazon, Madeira and Negro rivers).

To get around hypothesis 1, the authors tested whether the timing of divergence events were congruent with a single episode of vicariance associated with barrier formation, the Andean uplift. To test hypothesis 2, they compared the different dispersal abilities of lineages to their diversification rate. The idea being that species with lower dispersal abilities accumulate higher genetic differentiation between populations, which, in turn, leads to higher speciation rates. The measures of dispersal are based on “foraging stratum (a measure of dispersal ability linked to the behavior of birds: canopy, high dispersal ability or understory, low dispersal ability) and niche breadth (an indirect measure of dispersal ability based on habitat preference)”.

Birds included in the study. Bird drawings from Smith et al. (2014), originally from del Hoyo et al. (2013) Handbook of the Birds of the World.

Birds included in the study.
Bird drawings from Smith et al. (2014), originally from del Hoyo et al. (2013) Handbook of the Birds of the World.

What their genetic data indicate is that there was not a single divergence event, but rather between 9 and 29, and the timing of these events were not synchronous. Most of the species diversity originated during the Pleistocene, i.e. after the Neogene formation of the landscape matrix. If any of the vicariance events predicted to affect speciation (Andean uplift, Isthmus of Panama, Amazonian rivers formation) had been the source of the diversification, the lineage divergence time would be synchronous, since they were being affected by the same event, considering these are relatively recently divergent species. However, wouldn’t only older divergence events be affected by old vicariance events? How well we can test this is entirely dependent on how well the old phylogenetic node divergences can be estimated. In the paper, the authors acknowledge that they “… do not reject the possibility that the initial geographical isolation of populations at deeper phylogenetic scales was due to vicariance associated with the Andean orogeny or with the emergence of other landscape features”.

“Although highly suggestive of multiple dispersal events, this variation could be explained by a single vicariant event associated with the Andean uplift if the dispersal restrictions imposed by the barrier were heavily dependent on dispersal ability, such as was reported for a taxonomically diverse group of marine organisms isolated by the formation of the Isthmus of Panama. In a similar fashion, the emerging Andes could have first become a barrier for bird lineages with low dispersal abilities, with fragmentation of the distributions of more dispersive lineages occurring later. However, we detected no significant associations between dispersal abilities and divergence times across the Andes and the Isthmus of Panama that would support a model of ecologically mediated vicariance for these barriers.”

What about hypothesis 2? They found that whether a bird lineage inhabits canopy or understory affected the species diversity of that lineage. Since they used foraging strata as a proxy for dispersal ability, this result corroborates with the idea that dispersal-limited lineages (occupying forest understory) are significantly more diverse. The longer a lineage has persisted through time was also a good predictor of species diversity, i.e., older lineage accumulated more differentiation.

“The accumulation of bird species in the Neotropical landscape occurred through a repeated process of geographical isolation, speciation and expansion, with the amount of species diversity within lineages influenced by how long the lineage has persisted in the landscape and its ability to disperse through the landscape matrix.”

All in all, the paper doesn’t refute the vicariance hypothesis, but highlights the role of dispersal. These findings add to the ever-increasing pile of possible explanations for the higher diversity of the tropics and its heated discussion.

Smith, Brian Tilston, John E McCormack, Andrés M Cuervo, Michael J Hickerson, Alexandre Aleixo, Carlos Daniel Cadena, Jorge Pérez-Emán, et al. 2014. “The Drivers of Tropical Speciation.” Nature, September. doi:10.1038/nature13687.

Males can be the fragile sex for Leishmania parasites: sex-biased disease incidence in human populations of central Amazonia

When it comes to sex differences on the incidence of cutaneous leishmaniasis, male bias can exist even when exposure time is comparable among men and women.

Cutaneous leishmaniasis is a vector transmitted disease characterized by skin lesions that develop near or at the bite site of the vectors. Image from http://upload.wikimedia.org/wikipedia/commons/c/ca/Cutaneous_Leishmaniasis.jpg.

Cutaneous leishmaniasis is a vector transmitted disease characterized by skin lesions that develop near or at the bite site of the vectors. Image from wikipedia.

Cutaneous leishmaniasis (CL) is a tropical neglected disease that occurs in Central and South America, as well as in some regions of the African continent and the Middle East. Ulcerative lesions that develop at or near the vector’s bite site typically characterize CL, which is caused by parasites of the genus Leishmania, and transmitted by phlebotominae sand flies. According to the World Health Organization (WHO), in 2013 there were almost 100 thousand new cases reported all over the world. CL is considered a neglected disease because its mitigation receives less effort than it should, since the disease does not cause mortality. However, individuals presenting sings and symptoms of CL usually live in impoverished regions, can suffer from social exclusion because of the cutaneous nature of the lesions, besides having do deal with a medical treatment that can cause severe and debilitating side effects.

Cutaneous leishmaniasis incidence is lower among females, even when exposure time is comparable between sexes. This suggests the influence of endocrine-related immune factores, which make females better equipped agains parasitic infections. Image: Bettmann/CORBIS

Cutaneous leishmaniasis incidence is lower among females, even when exposure time is comparable between sexes. This suggests the influence of endocrine-related immune factors, which make females better equipped against parasitic infections. Image: Bettmann/CORBIS

In South America, the disease cycle is mainly sylvatic, meaning that humans are accidental disease hosts. Generally, in forested areas, sand flies would feed on sloths, armadillos and other small mammals, and humans would get occasionally infected if they were exposed to habitats where both vectors and wild hosts are found. Since men are usually the ones that engage in activities that involve being in contact with habitats where transmission is likely, such as hunting and logging, disease incidence tends to be higher among males than their female counterparts.  However, experimental infections in mice has also revealed that females, not only tend to develop the disease less often than males, but also present less severe lesions when clinical symptoms are present. Hence, one can ask whether male-biased disease incidence is solely due to differential exposure or is also a consequence of sex-related differences in the immune ability to cope with Leshmania spp. infection.

That was exactly the question I tackled for my MSc thesis research in the Instituto Nacional the Pesquisas da Amazônia. The study was just published on line in the journal Tropical Medicine and International Health, in which we investigated whether sex-biased CL incidence levels off when exposure time to CL vector habitats is comparable among sexes. We compared disease incidence between two populations from central Amazon: one composed by rural settlers, where exposure is male biased; and other composed by field researchers of the Biological Dynamics of Forest Fragments Project, where both males and females are similarly exposed to forested environments. Interestingly, at low levels of exposure disease incidence is higher among males in both populations, suggesting the existence of a sex-related and endocrine-mediated immunity against these parasitic infections. However, as exposure time increases, this suggested effect of higher immunity among females wears off, and disease incidence becomes comparable among sexes. Another relevant finding was that CL incidence among field researchers is eleven times higher than among rural settlers, which brings to attention a new disease risk group that deserves awareness.

This study was advised by Dr Gonçalo Ferraz, and co-advised by Dr Fernando Abad-Franch, in a collaboration between the Instituto Nacional de Pesquisas da Amazônia (INPA), the Biological Dynamics of Forest Fragments Project (INPA/Smithsonian Tropical Research Institute), and the Instituto Leônidas e Maria Deane (FIOCRUZ-AM).  I am very grateful to all of those who answered my epidemiological questionnaire and made this study happen!

Soares, L., Abad-Franch, F. and Ferraz, G. (2014), Epidemiology of cutaneous leishmaniasis in central Amazonia: a comparison of sex-biased incidence among rural settlers and field biologists. Tropical Medicine & International Health. doi: 10.1111/tmi.12337

Invasive species can take advantage of habitat changes promoted by ecosystem engineers

The Asiatic oak weevil, an invasive beetle with the potential to alter forest composition, takes advantage of shelters built by leaf-tying caterpillars in oak trees.

The Asiatic oak weevil takes advantage of leaf tying shelters built by caterpillars in oak trees.

The Asiatic oak weevil takes advantage of leaf tie shelters built by caterpillars in oak trees. Photo by Steve Nanz.

Ecosystem engineers are species capable of altering the environment and creating new habitats for other species. Beavers are the most popular ecosystem engineers – their shelters create dams that extend wetland areas, facilitating the colonization of aquatic plant species and other vegetation-associated organisms. Because of their role in enhancing habitat heterogeneity and promoting local species diversity, ecosystem engineers should be important targets for promoting the conservation of species and ecosystems. However, for every rule there is an exception. Even though ecosystem engineers can be positively associated with the establishment of local diversity, now there is evidence that invasive species can also take advantage of the habitat modification promoted by these natural engineers.

A hair clip was used by Baer and Marquis to artificially simulate caterpillar leaf tie shelter. Photo by Robert J Marquis.

A hair clip was used by Baer and Marquis to artificially simulate caterpillar leaf tie shelter. Photo by Robert J Marquis.

In a study that just came out in the Ecology journal, Baer and Marquis use an experimental approach with artificial caterpillar shelters to investigate the effects of ecosystem engineering on the abundance and host preference of the invasive beetle Cyrtepistomus castaneus, known as the Asiatic oak weevil. Oak trees are the favorite meal of C. castaneus; the weevil larvae eat the roots and the adults consume the leaves of these tree species. Although differences in leaf quality among different species of oaks influence the host-tree preference of weevils, the presence of leaf-ties was proven to have a positive role on the abundance of this invasive beetle species. The study not only explains what factors drive C. castaneus to explore certain species of oaks, but also sheds light on the relevance of ecosystem engineers in promoting the invasion of a forest habitat by a non-native species. Invasive species often have a set of conditions in common that facilitates initial establishment in a new environment, such as flexible resource usage and high reproductive rates. It is undetermined whether ecosystem engineers have a decisive role on facilitating initial ecosystem colonization of invasive weevils, and even other invasive species. However, weevils are not the only ones that benefit from these ecosystem engineers, since it is known that caterpillars that produce leaf tie shelters also increase the diversity of native arthropods.

 Even though people usually think about invasive species succeeding because they find new food and avoid old enemies, it may also depend on how helpful their new neighbors are” – Christina Baer

Baer CS & Marquis RJ. 2014. Native leaf-tying caterpillars influence host plant use by the invasive Asiatic oak weevil through ecosystem engineering. Ecology (in press).

Deforestation weakens social mutualism in Amazonian avian mixed-species flocks

Data from almost 1000 hours of observation reveal the detrimental effects of deforestation on non-trophic interspecies interactions among avian mixed-species flocks. 

Cinereous antshrike is the core of Amazonian avian mixed-species flocks – they rally individuals of other species and perform alarm calls. Photo by Letícia Soares.

Cinereous antshrike is the core of Amazonian avian mixed-species flocks – they rally individuals of other species and perform alarm calls. Photo by Letícia Soares.

Birds that form mixed-species flocks benefit from high efficiency on finding food and avoiding predation. Hence, avian mixed-flocks are cohesive social groups, and the evolutionary success of within-flock interactions is based on the idea that ‘those who remain together thrive together’. In the Amazon forest, flocks are usually composed by 8-10 different insectivorous species that can be represented by a single individual, a mated pair or a family group. Species may present distinguished roles in the flock, and the most remarkable role is played by the Cinereous antshrike (Thamnomanes caesius) that performs alarm calls, as well as calls to gather individuals to flock. This mutualism also thought to contribute to increase local species diversity, since closely related species will more likely  be members of different flocks.

 

Avian mixed-species flocks are cohesive social groups, in which individuals benefit from enhanced high efficiency on finding food and avoiding predation. This figure depicts the network of interaction in a Amazonian mixed flock, with cinereous antshrike in the center, as the core species in the flock.

This figure depicts the network of interaction in an Amazonian mixed-species flock, with cinereous antshrike in the center, as the core species in the flock. Figure by Karl Mokross.

The beauty of this mutualism, and its usefulness in maintaining species diversity are being threatened by deforestation. In a study published last month in Proc B, Mokross & colleagues use network analysis to show that the cohesion and stability of Amazonian avian mixed-flocks are dramatically affected by deforestation. Flocks from small forest fragments and degraded forest patches not only have fewer species, but also present weaker associations, when these are present at all. The study highlights how the structure of ecological communities can be dramatically affected by non-trophic species interactions, and provides the alarming proof of how detrimental deforestation is for such network.

 

“The flocks completely disappeared from the deforested areas. The craziness about this is that even later on, after 30 years of forest regeneration, the interactions remain weak. In other words, there are flocks, but the species spend less time together.” – Karl Mokross

 

Example of networks and habitat configurations for three flocks found in primary forest, 10 ha fragment and secondary forest habitat types in the Brazilian Amazon. Differences in network structure reflect the decay of interspecific interactions in mixed-species flocks across a disturbance gradient. Edge thickness and transparency in each network are proportional to numbers of interactions. Interaction values at the lowest 10% are set to transparent. Nodes sizes are proportional to flock attendance.Figure and adapted caption from Mokross et al, 2014.

Example of networks and habitat configurations for three flocks found in primary forest, 10 ha fragment and secondary forest habitat types in the Brazilian Amazon. Differences in network structure reflect the decay of interspecific interactions in mixed-species flocks across a disturbance gradient. Edge thickness and transparency in each network are proportional to numbers of interactions. Interaction values at the lowest 10% are set to transparent. Nodes sizes are proportional to flock attendance. Figure and adapted caption from Mokross et al, 2014.

Karl Mokross, Thomas B. Ryder, Marina Corrêa Côrtes, Jared D. Wolfe, and Philip C Stouffer. Decay of interspecific avian flock networks along a disturbance gradient in Amazonia. Proc R Soc B 2013 281: 20132599

Darwin’s finches “reversing” their famous process of speciation

In a paper published this week on the American Naturalist, Kleindorfer et al. report on how one of the subgroups of Darwin’s finches, the insectivorous tree finches, are collapsing back via hybridization, and also suggest the extinction of the large tree finch, Camarhynchus psittacula.

The Darwin finches are some of the most iconic examples of adaptive evolutionary radiation, and consequently, speciation. There are some curious facts about the history behind Darwin’s finches that I think are interesting to share. History that which obviously involves our beloved blog namesake, Mr. Darwin.

Darwin finches, from Wikipedia.

Darwin finches, from Wikipedia.

Charles Darwin was known for his likings of hunting and avidity in collecting, and perhaps for that reason I always pictured Darwin happily shooting all kinds of finches in Galapagos and instantly recognizing how that was a major find, and making all the intricate connections between adaptive morphology and speciation. However, it was another shipmate of the Beagle, Syms Covington, who did most of the bird collections in Galapagos.

As with almost all breakthroughs, the “eureka” moment of this famous Darwin episode was an afterthought. Darwin didn’t even discuss the finches in the diary of his voyage on the Beagle at much length. At the time, Darwin thought those were blackbirds and gross-beaks. Only after being back in England is when the famous ornithologist John Gould identified those Galapagos birds as “a series of ground finches which are so peculiar [as to form] an entirely new group, containing 12 species.” After Gould had made his findings public is when Darwin associated their incredible morphological adaptation to the species divergence concept, when he noted that “seeing this gradation and diversity of structure in one small, intimately related group of birds, one might really fancy that from an original paucity of birds in this archipelago, one species had been taken and modified for different ends”. Also interesting is that, nowadays, we know Darwin’s finches diverged from a group of Tiaris birds, which originated in the Caribbean islands and then spread to Central and South America, and finally to the Galapagos.

Now, to add to their glorified fame as teachers of the workings of evolution, Darwin’s finches are showing us a snapshot of the reverse process. The paper of Kleindorfer et al – just hot off the presses on the American Naturalist (Feb. 24th) –  looked at the three Camarhyncus species, known as tree finches, in one of the Galapagos islands, Floreana, to test the mechanisms and functions of annual patterns of hybridization in these sympatric species.

Images of three sympatric tree finches from Floreana Island in 2010. A, genetic population 1; B, hybrid tree finch; and C, genetic population 2. From Kleindorfer et al (2014).

Images of three sympatric tree finches from Floreana Island in 2010. A, genetic population 1; B, hybrid tree finch; and C, genetic population 2. From Kleindorfer et al (2014).

“The three Camarhyncus species on Floreana Island are of special interest because Lack (1947) singled them out as a paradigmatic example of successful speciation in Darwin’s finches. The medium tree finch probably originated from a “small morph” of the large tree finch from Isabela Island, which was either followed by (Lack 1947) or preceded by (Grant 1999) separate colonization events of “large morph” large tree finches from Santa Cruz Island and small tree finches from another island. […] Evidence that we present here, however, suggests that these three species may represent a case of evolution in reverse …”

They had birds collected at three different time periods, 1900s, 2005, and 2010.  Their morphological and genetic analyses suggest that through time, species composition started to move away from the three distinct clusters (small, medium, and large), and by 2010, there were two species left, the small and the medium tree finches, along if a population of hybrids between the two.

“The results presented here go to the heart of evolutionary biology: by what criteria do we denote species, and by what criteria do new species form or collapse? Here we present evidence that three sympatric species of Darwin’s tree finches in the 1900s have collapsed, under conditions of hybridization, into two species by the 2000s.”

They argue that their results show a case of disassortative mating, where the females of the “small tree finches” (Camarhynchus parvulus) are choosing among the larger of the “medium tree finches” (Camarhynchus pauper), creating a hybrid population of intermediate morphology. As for the “large tree finch” species, Camarhynchus psittacula, they don’t appear in any of their collections during the 2000s, and authors suggest there is a chance the species has gone extinct.

Fido listens like you do

Humans and dogs similarly use the brain’s auditory cortex to process the acoustical cues related to emotions expressed in the human voice.

This is my dog Walter after having heard my negative answer for his "give me your cupcake" request.

This is my dog Walter after having heard my negative answer for his “give me your cupcake” request.

Sometimes, I ask my dogs a question, examine the look in their faces, and end up verbalizing the answer for them. Besides having indescribable fun doing it, I do that kind of weirdness because, as any other dog owner, I can swear they understand me – and now, there is scientific proof that we at least are at the same page in terms of voice processing. A study using functional magnetic resonance imaging (fMRI) compared the responses of dogs and humans to three types of sounds: human voice, dog vocalization, nonvocal sounds. The results suggest that not only dogs and humans share common functions in terms of voice processing, but also that, in humans, an specific area of the temporal lobe ‘prefers’ non-human vocalizations. Although the authors don’t discard the possibility that the similarities in the voice processing in the dog and human brain are due to convergent evolution, they suggest that such similarities might have been already present in the common ancestor of dogs and humans, about 100 million years ago. Thousand of years of domestication might be the reason why dogs present the same left gaze bias that humans do when reading facial expressions, but the fact humans and dogs process voices in a similar fashion might be one of the explanations for such a successful (and cozy) interaction.

Andics et al. 2014. Voice-Sensitive Regions in the Dog and Human Brain Are Revealed by Comparative fMRI. Current Biology (in press).

Study subjects during fMRI. Pictures from Adics et al. 2014.

Study subjects during fMRI. Pictures from Adics et al. 2014.

Global deforestation disclosed (literally)

Open access spatial data for global forest cover change reveals the dynamics of de- and re- forestation for the first decade of the 21st century.

Forest lost and gain data for the entire globe is now freely available, and in an accessible way for the general public. The Landsat satellite images reveal striking data on the trends of forest lost across countries and eco regions. A total of 2.3 million km2 of forests were lost worldwide between 2000 and 2012, and Tropical forests, especially South American forests, make up to 32% of the total forest lost, with a scaring deforestation rate of 2,101 km2 per year. Brazil’s policies against deforestation in the Amazon forest are thought to be the ones responsible for the fact the country had the largest decline in deforestation rate, amongst all other countries in the globe. Although Brazil is still in the second place in terms of gross forest lost, the recorded decrease in forest loss is definitely good news.

The work, published last November in Science, is now available at: http://earthenginepartners.appspot.com/science-2013-global-forest. The study resulted from the collaboration between the University of Maryland, State University of New York, USGS, Geographic Information Science Center of Excellence NASA, and Google Inc.