Shrew-opossums, our strangest mammals

The shrew-opossum Caenolestes sangay, not exactly cute and cuddly! Photo: Jorge Brito.

Most mammals, including us, are placental mammals. There are two smaller groups of mammals: egg-laying monotremes like the platypus, and marsupials like the opossum and kangaroo. These groups diverged more than a hundred million years ago from the lineage that became the placental mammals, and though they are minor players in the world today, both were more important in the distant past.  Marsupials in particular were once much more important and much more diverse. Marsupials apparently originated in the northern continent that became Asia and North America. About 65Mya marsupials moved from North America into South America, which at this time was also connected to Antarctica and Australia. Around 50-35Mya, at least one species of marsupial made it to what is now Australia via Antarctica, setting the stage for the later diversification of marsupials on that continent as it moved away from Antarctica and into its splendid isolation in the remoteness of the Pacific Ocean.

South American saber-toothed marsupial carnivore Thylacosmilus. Photo: Wikipedia CC.

Fossil evidence shows that ancient South America of 10-40Mya had a rich and ecologically diverse marsupial fauna. Some of them were the size of bears, and others were large predators with two saber-like teeth like those of the famous saber-toothed cats. Some were hopping animals similar to the kangaroo rat, some resembled the present-day North American opossum, and some were arboreal animals resembling primates. There was also a rich and varied group of small and mid-sized rat-like marsupials belonging to the order Paucituberculata, which included both carnivorous and plant-eating genera.

Over time, these strange marsupials slowly disappeared. Only a few species in the order Paucituberculata, and one species (or species complex) in the order Microbiotheria (which may have been  a reverse migrant from the early marsupial diversification in Australia), survive today.

Our reserves protect two of these survivors, the “shrew-opossums” Caenolestes convelatus in our Dracula Reserve and Caenolestes sangay in our Cerro Candelaria Reserve (see Technical Note 1 below). Both shrew-opossums are in the order Paucituberculata and both are mainly predators, feeding on insects, other arthropods, worms, frogs, and small mammals, but they also sometimes eat fruit and fungi. They have two distinctive lower incisors that point straight ahead, like daggers. Caenolestes sangay is a new species described in 2013 by a group of scientists that included our collaborator Jorge Brito. It is exciting to add a previously unknown descendant of this lonely lineage, which diverged from other marsupials 55Mya.

Caenolestes sangay skull, note the dagger-like lower incisors. From Ojala-Barbour et al (2013) A new species of shrew-opossum (Paucituberculata: Caenolestidae) with a phylogeny of extant caenolestids, Journal of Mammology 94: 967-982.

The shrew-opossum Caenolestes sangay. Photo: Jorge Brito.

The shrew-opossum from our Dracula Reserve, Caenolestes convelatus. Photo: Jorge Brito.

In our Dracula and Cerro Candelaria reserves, the resident species of Caenolestes is the sole representative of its order, and this makes its conservation especially important. Conservationists tend to think in terms of species diversity, but we should also pay attention to higher-level diversity. All else being equal, a reserve that contained sloths, manatees, monkeys, bats, and deer would be far more important than a reserve that protected only a set of rodents, even if the number of species were the same in each of the two reserves. A reserve with one species of rat and one species of shrew-opossum is far more diverse and important than an otherwise identical reserve with two species of rat and no species of shrew-opossum. The first reserve protects more unique evolutionary history than the second. I believe this should be the guiding principle of conservation: maximize the amount of unique evolutionary history protected.

Phylogenetic tree of the major mammal groups (orders). The order Paucituberculata, which contains the shrew-opossums, is highlighted in red. Modified from https://www.palaeontologyonline.com/articles/2012/fossil-focus-marsupials/

The amount of unique evolutionary history represented in a given locality is called its “phylogenetic diversity”. In this age of DNA analysis we have reasonably accurate phylogenetic trees for many plant and animal groups. For any given natural group — mammals, for example — the simplest measure of the amount of unique evolutionary history protected at a locality is the total length of all the branches in the phylogenetic tree (including the “trunk” that connects the group to the rest of the organisms in the reserve) of the species found there (see Technical Note 2 for other ways of measuring this). In the case of our shrew-opossum, it has been evolving on its own unique branch for at least 55 million years, so it contributes quite a lot of  phylogenetic diversity to our Cerro Candelaria and Dracula reserves. The shrew-opossums are among the most interesting mammals in our reserves, even though almost no one has ever heard of them.

Lou Jost, Fundacion EcoMinga

Technical notes:

1. The name “Shrew-opossum” can be misleading. Strictly speakimg, the opossums are marsupials in a different order than this animal. I think a better English name for these would be “marsupial shrew”.

2. My colleagues Anne Chao, CH Chiu, and I have developed some more advanced measures of phylogenetic diversity and differentiation: Chao A, Chiu CH, Jost L (2010) Phylogenetic diversity measures based on Hill numbers, Philosophical Transactions of the Royal Society B 365:3599–3609 https://www.researchgate.net/publication/47566303_Phylogenetic_diversity_measures_based_on_Hill_numbers

Zarigüeyas-musaraña, nuestros mamíferos más extraños 

IMG 01 – ¡La zarigüeya-musaraña Caenolestes sangay, no exactamente tierna y mimosa *delicada*! Fotografía: Jorge Brito 

La mayoría de mamíferos, incluyéndonos, son mamíferos placentarios. Hay dos grupos más pequeños de mamíferos: los monotremas pone-huevos como el ornitorrinco, y los marsupiales como las musarañas y el canguro. Estos grupos divergieron hace más de cien millones de años atrás del linaje que se volvió de los mamíferos placentarios, y aunque son jugadores menores en el mundo de hoy, ambos fueron más importantes en el pasado distante. Los marsupiales en particular fueron mucho más importantes y mucho más diversos. Aparentemente los marsupiales se originaron en el continente norte que se volvió Asia y Norteamérica. Cerca de 65 millones de años atrás los marsupiales se movieron de Norteamérica a Suramérica, lo cual en ese tiempo también se conectaba a la Antártica y Australia. Cerca de 50-35 millones de años atrás, al menos una especie de marsupial llegó a lo que ahora es Australia a través de la Antártica, preparando el terreno para una diversificación tardía de marsupiales en ese continente a medida que se alejaba de la Antártica y se adentraba en su espléndido aislamiento en la lejanía del Océano Pacífico.  

IMG 02 – Carnívoro marsupial dientes de sable sudamericano Thylacosmilus. Fotografía: Wikipedia 

La evidencia fósil muestra que la antigua Suramérica de hace 10 a 40 millones de años tenía una fauna marsupial rica y ecológicamente diversa. Algunas de ellas tenían el tamaño de osos, y otros eran grandes predadores con dos dientes en forma de sable como los de los famosos felinos dientes de sable. Algunos eran animales saltarines similares a la rata canguro, y algunos parecían a las musarañas norteamericanas de hoy en día, y algunos eran animales arbóreos parecidos a primates. También había un grupo rico y variado de marsupiales similares a ratas de tamaño pequeño y mediano pertenecientes al orden Paucituberculata, el cual incluye géneros carnívoros y herbívoros.  

A lo largo del tiempo, estos marsupiales extraños desaparecieron lentamente. Sólo unas pocas especies en el orden Paucituberculata, y una especie (o complejo de especies) en el orden Microbiotheria (el cual puede haber sido un migrante inverso de la diversificación marsupial temprana en Australia), sobrevive hoy. 

Nuestras reservas protegen dos de estos sobrevivientes, las “musarañas-zarigüeyas” Caenolestes convelatus en nuestra Reserva Drácula y Caenolestes sangay en nuestra Reserva Cerro Candelaria (ver la Nota Técnica 1 a continuación). Ambas zarigüeyas-musarañas están en el orden Paucituberculata y ambos son principalmente depredadoras, alimentándose de insectos, otros artrópodos, gusanos, ranas, y pequeños mamíferos, pero ellos también a veces comen frutas y hongos. Ellos tienen dos incisivos inferiores distintivos que apuntan hacia adelante, como dagas. Caenolestes sangay es una nueva especie descrita en 2013 por un grupo de científicos que incluyen a nuestro colaborador Jorge Brito. Es emocionante añadir un descendiente previamente desconocido a este linaje solitario, el cual divergió de otros marsupiales hace 55 millones de años.  

IMG 03 – Cráneo de Caenolestes sangay, observe los incisivos inferiores en forma de daga. De Ojala-Barbour et al. (2013) Una nueva especie de zarigüeya-musaraña (Paucituberculata: Caenolestidae) con una filogenia de caenolestidos existentes, Journal of Mammology 94:967-982 

IMG 04 – La zarigüeya-musaraña Caenolestes sangay. Fotografía: Jorge Brito 

IMG 05 – La zarigüeya-musaraña de nuestra Reserva Drácula, Caenolestes convelatus. Fotografía: Jorge Brito. 

En nuestras Reservas Drácula y Cerro Candelaria, la especie residente de Caenolestes es la única representante de su orden, y esto hace que su conservación sea especialmente importante. Los conservacionistas tienden a pensar en términos de diversidad de especies pero deberíamos también poner atención a la diversidad de alto nivel. En igualdad de condiciones, una reserva que contiene perezosos, manatís, monos, murciélagos y ciervos sería mucho más importante que una reserva que protege solo a un grupo de roedores, incluso si el número de especies fuera el mismo en cada una de las dos reservas. Una reserva con una especie de rata y una especie de zarigüeya-musaraña es mucho más diversa e importante que una reserva idéntica con dos especies de rata y ninguna especie de zarigüeya-musaraña. La primera reserva protege una historia evolutiva más singular que la segunda. Creo que este debería ser el principio rector de la conservación: maximizar la cantidad de historia evolutiva única protegida.

IMG 06 – Árbol filogenético de la mayoría de los grupos de mamíferos (órdenes). El orden Paucituberculata, el cual contiene las zarigüeyas-musarañas, esta resaltado en rojo. Modificado de: https://www.palaeontologyonline.com/articles/2012/fossil-focus-marsupials/ 

La cantidad de historia evolutiva única representada en una localidad dada es llamada su “diversidad filogenética”. En esta era de análisis de ADN tenemos árboles filogenéticos razonablemente precisos para muchos grupos de plantas y animales. Para cualquier grupo natural dado – mamíferos, por ejemplo – la medida más simple de la cantidad de historia evolutiva única protegida en una localidad es la longitud total de todas las ramas en el árbol filogenético (incluyendo el “tronco” que conecta el grupo al resto de los organismos en la reserva) de las especies encontradas ahí (mire la Nota Técnica 2 para otras maneras de medir esto. En el caso de nuestra zarigüeya-musaraña, ha ido evolucionando por su propia rama por al menos 55 millones de años, de modo que contribuye bastante a la diversidad filogenética de nuestras reservas Cerro Candelaria y Drácula. Las zarigüeyas-musarañas están entre los mamíferos más interesantes en nuestras reservas, incluso aunque casi nadie ha oído hablar sobre ellas. 

Lou Jost, Fundacion EcoMinga 

Traducción: Salomé Solórzano-Flores

 

Notas Tecnicas: 

1. El nombre “zarigüeya-musaraña” puede ser engañoso. Estrictamente hablando las zarigüeyas son marsupiales en un orden diferente que este animal. Creo que un mejor nombre en inglés para esto podría ser “musaraña marsupial” 
2. Mis colegas Anne Chao, CH Chiu, y yo hemos desarrollado algunas medidas más avanzadas para la diferenciación y diversidad filogenética: Chao A, Chiu CH, Jost L (2010) Diversidad filogenética basada en los números de Hill, Philosophical Transactions of the Royal Society B 365:3599-3609 https://www.researchgate.net/publication/47566303_Phylogenetic_diversity_measures_based_on_Hill_numbers 

Two new scientific papers coauthored by EcoMinga staff

In the last few days two new papers were published which had EcoMinga staff as coauthors:

Magnolia vargasiana (Magnoliaceae), a new Andean species, and a key to Ecuadorian species of subsection Talauma, with notes in its pollination biology J. Antonio Vasquez-Garcia, David A. Neill, Mercedes Asanza & Luis Recalde

Eager to get the flower buds of these magnolias, Luis Recalde and Fausto Recalde climbed high into the canopy. Here Luis climbs the hemiepiphyte root hanging from the right-hand side of the magnolia trunk; click to enlarge since he is so high he is almost invisible. Photo: Lou Jost/EcoMinga.

Luis Recalde, one of our reserve caretakers whose photographic work appears often on this blog, was coauthor of this paper. It describes one of two new species of Magnolia discovered recently in our Rio Zunac Reserve. These Magnolias open mainly at night, so buds need to be collected from high in the canopy during the day and brought to earth for observation. Luis risked his life multiple times to obtain flower buds from the canopy of this tree, free-climbing a thick aerial root of a hemi-epiphyte growing high in the tree’s crown. The effort exhausted him, the first time I’d ever seen him tired.

Luis’ salary is financed by the World Land Trust’s “Keepers of the Wild” program, thanks to a donation to the WLT from Puro Coffee. Thanks very much, WLT and Puro!!

Expected Shannon Entropy and Shannon Differentiation between Subpopulations for Neutral Genes under the Finite Island Model Anne Chao, Lou Jost, T. C. Hsieh, K. H. Ma, William B. Sherwin, Lee Ann Rollins

This paper derives some fundamental results on the relationship between Shannon entropy and evolution. Shannon entropy is an important theoretical quantity in many sciences, including physics and information theory. It can be partitioned into within- and between-group components, and these components can be used to contruct a measure of the degree of genetic differentiation between two or more subpopulations of a species. Unlike previously-used measures of genetic differentiation, this one has mathematical properties that make it always increase when a gene in one subpopulation mutates into a new gene. That is how speciation starts–two subpopulations that don’t mix very much will gradually accumulate new mutations and so become genetically distinct. Thus the entropy-based measure of differentiation can accurately describe the beginnings of the speciation process.

But we’d like not only to merely describe the degree of differentiation between subpopulations, but to know the causal role of the genetic and demographic factors (subpopulation size, number of subpopulations, migration rate between subpopulations, mutation rate, strength of natural selection ) that control the process. To figure that out, geneticists use a simple mathematical model of the subpopulations, ignoring natural selection for now. This model is called the “finite island model”. Subpopulations that obey this model always reach an equilibrium amount of genetic differentiation that is completely determined by the genetic and demographic parameters of the model. The challenge, then, is to figure out the formula for the equilibrium amount of differentiation in terms of the model parameters.

The first step is to figure out a formula for the entropy of a single population at equilibrium. Some progress had been made on that problem by William Sherwin and his colleagues, but the breakthrough came when Anne Chao discovered that the entropy at equilibrium was given by a very elegant mathematical function (called the digamma function) of a certain combination of the model parameters. From there it was possible to formulate the entropy of a subdivided population, and the entropy of the subpopulations. And from this we could derive the entropy-based measure of genetic differentiation in terms of the model parameters. The result showed that under a broad range of conditions, the main factor determining the amount of differentiation at equilibrium was the ratio of migration rate to mutation rate. Under other conditions, other factors also had important effects. This result can help us better understand the mechanisms of speciation.

The paper contains many other interesting results, including a novel test to check if a set of genes is being acted on by natural selection, and a novel connection between different mutation models. Interested readers can get the paper free on PLoS1. I’d like to thank my coauthors for a really wonderful and productive collaboration. I’d also like to thank Tom Leinster and the Centre de Recerca Matematica, Universitat Autonoma de Barcelona, Catalunya, for hosting Bill and I as visiting fellows for a month and for bringing Anne as well to the wworld’s first Mathematics of Biodiversity conference there.

Lou Jost
http://www.loujost.com