How ancient river systems, geological barriers and climatic changes in the Western Ghats influenced speciation of balitorid loaches

Of the many endemic and evolutionarily distinct freshwater fish lineages of the Western Ghats Biodiversity Hotspot, the mountain loach genus Bhavania comprises a biogeographically fascinating group. Its morphological similarities to the sucker-loaches of Indo-China and Sunda Islands had fuelled speculations that this group originated from South East Asia, and colonized the Western Ghats during the Pleistocene. Despite being known since the 1840s, there were no efforts until this date, to understand the how this group of fishes evolved and diversified in the region.

(Above) The mountain loach, Bhavania australis is a ‘cryptic species complex’ endemic to the Western Ghats Biodiversity Hotspot in India. Photo credit: Beta Mahatvaraj. Mexico.

Most importantly, the apparent wide distribution of the genus in the Western Ghats from 9° to 13°N latitudes (an approximate south-north distance of 450 km), and the fact that only two species were known, encouraged us to investigate the true diversity within this genus. After our team carried out extensive sampling in torrential mountain tributaries of 16 river systems of the Western Ghats, collecting specimens which were then subjected to molecular phylogenetic and biogeographical analysis, the results did not surprise us.

COVER ARTICLE:
Sidharthan A, Raghavan R, Anoop VK, Philip S & Dahanukar N (2020) Riddle on the riffle: Miocene diversification and biogeography of endemic mountain loaches in the Western Ghats Biodiversity Hotspot. Journal of Biogeography 47, 2741-2754. https://doi.org/10.1111/jbi.13972

The genus Bhavania was shown to harbour many more species than previously known. Molecular genetic analysis revealed that the currently known Bhavania australis represented a ‘species complex’ comprising six or seven putative species, with restricted distribution ranges. This has now helped us to better understand their extinction risk, and inform future conservation action.  Unfortunately, naming them has become a challenge, as they are cryptic and hard to tease apart morphologically!

Collecting mountain loach.

We also found that these mountain loaches originated in the early Neogene, and subsequently diversified in the Miocene, and later in the Pliocene and Pleistocene. This laid rest to the speculations of early Indian ichthyologists, and biogeographers that these fishes originated in South East Asia and arrived into India in the Pleistocene. The current distribution pattern of these mountain loach species on the different hill-ranges and its associated drainages in the Western Ghats reflect the climatic (intensification of monsoonal rains) and physiographic (aridification, formation of land barriers, drying up of riverine connections, and fragmentation of streams) changes that could have occurred on this mountain during the Miocene. Together these would have resulted in dispersal of these loaches to new areas, and isolation in others, leading to the current pattern of diversity and distribution. A highlight of our study was what could be the first evidence for a large river system (the Cauvery) facilitating an east-west pathways for dispersal and diversification of endemic fish species of the region.

As a next step, we are embarking on an ambitious project to investigate the global phylogeny and biogeography of balitorid loaches so as to help improve our understanding of the evolution and diversification in this fascinating family of mountain loaches.

Written by:
Arya Sidharthan (1) and Rajeev Raghavan (2)
^{(1) PhD Candidate, School of Ocean Science and Technology, Kerala University of Fisheries and Ocean Studies, India; Assistant Professor, Department of Fisheries Resource Management, Kerala University of Fisheries and Ocean Studies, India.}

Additional information:
@LabRajeev @AryaSidharthannswick www.fishlab.in

Corroborating, refining, or refuting species’ modelled historical distributions can require innovation in datatypes and the synthesis of diverse kinds of information from sometimes unexpected sources.

Ecological niche and species distribution models are tools currently applied in several fields of biology and other disciplines. These models use algorithms to correlate species presence data with environmental layers to reconstruct ecological niches. Ecological niches can then be projected into a geographic space and time, which enables us to make a hypothesis about the potential species distribution.

(Above) Rock art depiction of a desert bighorn sheep
from Sierra de San Francisco, Baja California, Mexico.

We have long been interested in the reconstruction of vertebrate distributions at different spatial and temporal scales. Obtaining their current potential distributions is relatively simple since it is the period where we have more data on the species presence. However, when faced with palaeo-distributions, we can only reconstruct the ecological niches of species in the present and project them to past climate scenarios. This has drawbacks, for example we do not know if the reconstruction of the current niches is well represented. Additionally, we must assume those niches did not change over the projected period of time (also known as niche conservatism).

EDITORS‘ CHOICE: (Read for free until Feb 2021):
Gámez‐Brunswick, C, Rojas‐Soto, O. New insights into palaeo‐distributions based on Holocene rock art. J Biogeogr. 2020; 47 (12): 2543–2553. https://doi.org/10.1111/jbi.13975

One day we stumbled upon a magazine that had a piece about rock art and realized that we have had information from the past for a long time. Rock art has been there for thousands of years, talking to us, static, but telling very interesting stories. They tell us about the interaction of those prehistoric humans with species and their environment through incredible paintings and engravings in stone. Therefore, we could use rock art sites as records of the species represented in that time frame, and then model their distribution with modern day tools.

This seemed possible, but we had not yet realized all the difficulties; there is an enormous number of rock art sites in North America, and at each one there are several species depicted with varying degrees of detail. How is it that we could choose our species and reduce the identification error to a minimum? And moreover, how could we set a time range for all of the representations? Then, once inside the wonderful world of rock art, we found drawings of an ungulate that was very meaningful to hunters, with easily identifiable backward-twisted horns and the only species in that range … the bighorn sheep.

Potential distribution of the desert bighorn sheep from Mid-Holocene (red) and present (grey) in two environmental dimensions (PCs) (left) and in a geographic space (right), as reconstructed from rock art (light orange squares) and current records (black points) respectively.

The bighorn sheep has a wide representation in North American rock art; its importance for so many cultures allowed us to obtain records captured in rocks both from northern Mexico and the southwestern United States. The complex task was to assign a date to all these depictions, and it was there that biology, anthropology, and archaeology collided. Thanks to the study of all those prehistoric human settlements, we were able to assign them a space in our timeline, and thus achieve a match with the environmental layers of the Mid Holocene (6,000 years ago). With this, we were able to model the niche of the bighorn sheep in the past and make comparisons with its data from the present, which we already had very well represented.

The importance of this analysis is in the use of records that were illustrated in rock art for so long and had been overlooked. Furthermore, it allowed us to demonstrate for the first time that niche conservatism does exist in time periods such as the one that separates us from the Mid Holocene. With this, we open the opportunity to start a line of study where we can delve more precisely into palaeo-distributions; particularly in the face of an extremely scarce fossil record. The analysis of species niches and their distributions over time gives us the possibility to understand their temporal dynamics and with this, to better understand the environmental changes that we are already beginning to suffer and will only increase in the future with climate change.

Written by:
Carolina Gámez-Brunswick & Octavio Rojas-Soto
^{Laboratorio de Bioclimatología, Red de Biología Evolutiva, Instituto de Ecología A. C.}

Additional information:
@carobrunswick

We use landscape data to understand spatial patterns of diversity of one of the smallest groups of insects: thrips. The study was performed in Reunion island, a small volcanic island of the Indian Ocean. The dramatic changes in elevation, abiotic conditions and anthropisation allowed us to explore multiple variables affecting diversity revealing why, despite more than a century of research, the elevational diversity gradient is far from being fully understood.

How diversity is distributed on our planet is one of the patterns that has been most intensely studied by ecologists. One such pattern is the change in diversity along elevational gradients, which was already noticed by Alexander von Humboldt in the 18th century. Since then many studies have tried to find general rules behind this gradient, but the more the pattern is studied the more complex it seems to be. The reasons are many and include that the elevational diversity gradient depends on both abiotic conditions and biotic interactions, it may change with latitude, taxa or climatic regions, and the relationship is not always linear with diversity being often larger at mid-elevations. In addition, human impacts on ecosystems also co-vary with elevation with concomitant effects on diversity. Early researchers were able to observe this pattern in pristine ecosystems, which are nowadays rare. Human activities are currently the strongest drivers of diversity erosion, and including these activities on the study of diversity gradients can help to better understand spatial patterns of diversity.

(Above) Lentil crops embedded within the National Park in the Cirque de Cilaos, Reunion island.

Our study aimed to explore whether diversity changes along elevation could be better understood if human impacts on landscape structure were taken into account. We selected three important variables that can be obtained from highly-resolved vector layers: the amount of habitat available, habitat diversity, and fragmentation. The study was performed in Reunion, a small island in the Indian Ocean recognized as a diversity hotspot. This volcanic island offered a unique opportunity to test our hypotheses given its dramatic changes in elevation as well as at the landscape level. Low elevation areas are dominated by human settlements, mid elevation ones are mostly devoted to agriculture (and sugarcane in particular), and higher elevation areas are protected by a National Park. The study was done using as model system a group of minute insects known as thrips (Thysanoptera), and was part of Niry Dianzinga’s PhD, a project that required intense sampling and identification of thrips, with the new species Thrips reunionensis being discovered.

FROM THE COVER:
Dianzinga, N.T., M.-L. Moutoussamy, J. Sadeyen, L.H.R. Ravaomanarivo, & E. Frago (2020) The interacting effect of habitat amount, habitat diversity and fragmentation on insect diversity along elevational gradients.  J. Biogeogr. 47 (11): 2377-2391.  https://doi.org/10.1111/jbi.13959

The model system used in our study imposed an important challenge because, as far as we are aware, we were among the first to use this group of insects in a diversity study. It was rewarding to find out that a large part of the diversity of this group (a total of 40 species) could be obtained by sampling insects from flowers using the beating sheet technique, a simple, cheap, and quick method to sample insects. Despite many previous studies suggesting that these insects mostly disperse passively with wind currents, we found that they establish tight interactions with flowering plants, which may allow us to use this insect group to study insect-plant interaction networks in the future. This model is also interesting given its large functional diversity: most species are herbivorous, but several species feed on fungi, and some species are predators, like the species Franklinothrips vespiformis depicted on the cover of issue 47(11) of the Journal of Biogeography.

Savannah ecosystem in La Savane, Saint-Paul, Reunion island.

Our results are a good example of the challenges to understand the elevational diversity gradient because variables affecting thrips diversity were multiple, and often interacted in an intricate manner. During the rainy season, rainfall was one of the most important variables affecting insect diversity, but during the dry season elevation dominated. Among landscape variables, the amount of habitat available and its diversity were also important but one variable modulated the effect of the other: insect diversity increased with habitat diversity, but this effect was offset in areas of low habitat amount. Overall our results suggest that landscape effects can help us to better understand the elevational diversity gradient, but also that diversity may change a lot between seasons. Most research on diversity patterns has focused on spatial patterns, and we believe that temporal trends in diversity will provide exciting new knowledge on how diversity is maintained or lost. Temporal diversity trends may be particularly important to explore given the unprecedented loss of insect diversity occurring during the last decades.

Another important challenge for future studies will be to dig deeper into the landscape data that can be obtained from satellite imagery. In our study we obtained data from vector layers that were very accurate in delineating different land uses, but that did not distinguish, for example, vegetation types among the natural forest category, or did not provide any information on plant or soil diversity. It thus remains to be answered whether insect communities are more unique in areas where plant communities are unique too, or whether areas dominated by invasive or agricultural plans, are also dominated by exotic or pest insects. These questions will for sure provide a more detailed understanding of insect diversity patterns, but answering them will require intense field work that is not always possible. As it commonly happens in ecological studies, the balance between the quality of the information obtained, and the human endeavor needed to obtain such data will need to be evaluated depending on access to study sites, the questions asked, the model system and the funding available, among others.

Written by:
Enric Frago and Niry T Dianzinga
^{CIRAD, CBGP, Montpellier, France, and CIRAD-UMR PVBMT, Saint-Pierre, La Réunion, France.}

Additional information:
https://sites.google.com/site/enricfrago/home
@EnricFrago

Bois de corail, Chassalia corallioides, a Reunion endemic in the Cirque de Mafate that owes its name to the coral-like structure of the flowers

Local biological diversity, also known as alpha diversity, has three different components: the number of species in a given area (taxonomic diversity), the number of distinct traits that these species have (functional diversity) and their evolutionary distinctiveness (phylogenetic diversity). The relationships among these components of diversity vary across geography reflecting the differences in eco-evolutionary processes among distant regions.

(Above) 3D visualization of the empirical relationships between functional diversity, phylogenetic diversity and taxonomic diversity for amphibians in the Continental Americas based on our theoretical framework.

This study was motivated by the fact that different components of biological diversity have been shown to vary slightly in their geographical distribution: while species richness, phylogenetic diversity and functional diversity are broadly correlated, there are some regions where one measure of diversity is higher or lower than expected based on the others.

FROM THE COVER: Ochoa-Ochoa, LM, Mejía-Domínguez, NR, Velasco, JA, Dimitrov, D, Marske, KA. Dimensions of amphibian alpha diversity in the New World. J Biogeogr. 2020; 47: 2293– 2302. https://doi.org/10.1111/jbi.13948

We discussed extensively the possibilities to integrate these three dimensions of biological diversity in a single framework and developed a set of hypotheses about the potential drivers of variability in the relationships among the diversities.  We then mapped the spatial distribution of these diversity measurements and use our theoretical framework to explore the processes that may have generated the spatial patterns of amphibian diversity in the New World as we know it today.

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Quilticohyla zoque is a treefrog species from the family Hylidae
from Nahá reserve, Chiapas, Mexico. Photo: LMMO.

We found that although the three aspects of diversity showed similar patterns, the geographical variation in the relationship between diversities suggested that a variety of processes, including ecological opportunity, habitat filtering, competitive interactions, among others have had different impacts on the different components of diversity. We also found regional differences dominant processes shaping diversity patterns.

Finally, we concluded that neither dimension of amphibian alpha diversity is a general predictor for other dimensions. Thus a single explanation about ecological and evolutionary processes underlying geographical variation in amphibian diversity is not possible. Our findings have major implications for conservation because setting conservation priorities may require analyses to determine which is the most important dimension of diversity to be conserved. Thus, the question of whether to give priority to history (e.g., antique lineages, evolutionary uniqueness), to high functional diversity (with rare or unique functions) or to taxonomic diversity (number of species) is critical.

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Rhinophrynus dorsalis, is a Mexican burrowing toad from the family Rhinophrynidae
from Nahá reserve, Chiapas, Mexico. Photo: LMMO.

Ideally, if we want to preserve a wider range of the evolutionary spectrum, the aim should be, not only to conserve as many species as possible, but also to conserve a broad selection of different phylogenetic lineages and life history traits (functions). We expect that our findings will stimulate a new generation of local studies aimed at deciphering how diversity in ecological roles, evolutionary heritage and species numbers was assembled by ecological and evolutionary processes at finer spatial scales.

Written by:
Leticia Margarita Ochoa-Ochoa, Full Professor, Evolutionary Biology Department, Museum of Zoology, Faculty of Sciences, UNAM.
Nancy R. Mejía-Domínguez, Associated Researcher, Unidad de Bioinformática, Bioestadística y Biología Computacional, Red de Apoyo a la Investigación (RAI). Coordinación de la Investigación Científica, UNAM.
Julian A. Velasco, Associated Researcher, Centro de Ciencias de la Atmósfera, UNAM.
Dimitar Dimitrov, Associate Professor, Department of Natural History, University Museum of Bergen, University of Bergen, Bergen, Norway.
Katharine A. Marske, Assistant Professor, Geographical Ecology Group, Department of Biology, University of Oklahoma, Norman, Oklahoma, USA

For more information:
@Lety_OchoaOchoa /  http://academicos.fciencias.unam.mx/leticiaochoa/
@MejiaDNancy / https://sites.google.com/view/biostatisticsrai-unam/
@juvelas / https://www.atmosfera.unam.mx/ciencias-atmosfericas/cambio-climatico-y-radiacion-solar/julian-a-velasco-vinasco/
@spidersphylo / http://www.dimitardimitrov.name
@kamarske / Kamarske.org

Mouse-goats, ‘demons of the forest’, and other insular bovids have short and robust limbs. Why?  The ‘low gear’ hypothesis had never been tested until we decided to fill this gap with a quantitative investigation of the causal forces influencing the acquisition of this peculiar type of locomotion.

Above: Skulls of a tamaraw (Bubalus mindorensis), a dwarf buffalo endemic to Mindoro island, highlighting different stages of ontogenetic development (Mammal Collection; Field Museum of Natural History, Chicago).

The Dutch palaeontologist P. Y. Sondaar already noticed in the 1970s that many insular ruminants, and to a lesser degree insular elephants and hippopotamuses, exhibited short and robust limbs. He explained this as an adaptation for a peculiar type of gait, that he described and named ‘low gear’ locomotion. Sondaar and other researchers after him mentioned several examples, including the iconic Balearian mouse-goat (Myotragus balearicus). They believed that this stout structure of the limbs would be advantageous, in the absence of predators, for low-speed walking in mountainous environments.

Bovids are intriguing elements of insular faunas and encompass phyletic dwarfs that occurred or are still living on islands located in different regions, from Southeast Asia to the Mediterranean. I have previously investigated their body size evolution on islands, (https://onlinelibrary.wiley.com/doi/full/10.1111/jbi.13197) and we decided to concentrate on the bovid family again in this study. Some of the best-known cases of ‘low gear’ locomotion include the already mentioned Myotragus as well as the tamaraw, a living dwarf buffalo endemic to Mindoro in the Philippines. We focused on the two main morphological traits associated with this peculiar type of gait, that is short and robust metapodials, and we calculated response variables in 21 extinct and living insular bovids. We assembled data on their life history and ecology and on the physiography of 11 islands. We estimated 10 predictors, including 4 topographic indices, and assessed their contextual importance by combining statistical and machine learning methods.

FROM THE COVER: Rozzi, R, Varela, S, Bover, P, Martin, JM. Causal explanations for the evolution of ‘low gear’ locomotion in insular ruminants. J Biogeogr. 2020; 47: 2274– 2285. https://doi.org/10.1111/jbi.13942

We demonstrated that the evolution of ‘low gear’ locomotion in insular ruminants does not result simply from phyletic dwarfing and from the absence or scantiness of predators in the focal communities. Instead, we showed that release from competitors on species-poor islands plays an essential role in prompting adaptations for this peculiar type of gait. While island topography is not as relevant as interspecific dynamics in influencing the evolution of the focal morphological traits, the amount of mountainous terrain occurring on each island seems to significantly affect the evolution of robust metapodials in insular bovids. All in all, our study supports the idea that the evolution of ‘low gear’ locomotion would be the product of a complex interplay of biotic and abiotic factors, and calls for caution in drawing conclusions on this phenomenon on the basis of single, albeit significant cases.

(Left) Roberto measuring a skull of the iconic mouse-goat, Myotragus balearicus, at IMEDEA – Mediterranean Institute for Advanced Studies, Mallorca. M. balearicus was an endemic caprine that lived on Mallorca and Menorca during the Late Pleistocene and Holocene, before becoming extinct following the arrival of humans around 4300 years ago. (Right) Roberto embraced by the horns of a river buffalo, Bubalus bubalis, in the mammal collections at the Smithsonian National Museum of Natural History, Washington DC.

An unexpected outcome of this study was to find out that, even though the most extreme cases of ‘low gear’ locomotion occurred on islands with no mammalian predators, our models did not show a significant relationship with this predictor. To sum up, the a priori hypothesis that this low-speed gait would simply result from predator release on islands needed to be reconsidered. Discussing the role of ecological and topographic traits in influencing the evolution of ‘low gear’ locomotion was challenging, because of their complex interaction and the variation in morphological responses to those factors within insular bovids. In fact, we observed a variety of trait combinations, with species exhibiting different degrees of robustness and shortening of metapodials, and different responses to many of the focal predictors by species belonging to one or the other subfamily of bovids in the study.  Thus, much effort is still needed to verify how robust island syndromes are and to understand their causation. In this vein, I am planning to continue to explore other peculiar traits exhibited by these fascinating animals. In particular, I am looking forward to implementing advanced methodologies in palaeoneurology to investigate patterns of brain size variation and changes in the degree of cortical folding in insular Artiodactyla.

More broadly, my research focuses on the evolution and extinction of mammals on islands. There is some urgency to this.  In response to the special characteristics of island environments, these animals often undergo fascinating evolutionary changes, including changes in body size and in the morphology of their skull, brain, teeth and limbs. My collaborators and I are currently focusing on how the evolutionary changes undergone by insular mammals predispose them to heightened extinction risk. I am investigating the relationship between their peculiarity and their fragility, as many of these evolutionary marvels are often threatened or already extinct. In collaboration with other palaeontologists, mammalogists and biogeographers, we are integrating data on fossil and living insular mammals to document their extinctions across large scales of time and to inform conservation strategies.

Mounted skeleton of the extinct (Middle Pleistocene) Sicilian dwarf elephant
Palaeoloxodon falconeri at Museo Geologico ‘G. G. Gemmellaro’, Palermo, Sicily.

The application of theories and analytical tools of palaeontology to provide valuable information for conservation planning is one of the key drivers of my research. Many threatened island mammals receive scarce conservation action because they are deemed ‘uncharismatic’ and fail to attract funding. Palaeontological studies have the potential to produce detailed information on the evolutionary history and uniqueness of these species and, thus, draw attention to their conservation value. I did my PhD on insular bovids and I was saddened to read that, in a recent study on the full collection of mammals from the Prague Zoo, the lowland anoa (Bubalus depressicornis) was ranked as one of the least attractive species. Sometimes referred to locally as Sulawesi’s ‘demon of the forest’, anoas never cease to inspire my research and, as a member of the IUCN SSC Asian Wild Cattle Specialist Group (https://www.asianwildcattle.org/), I feel it is important to keep highlighting how beautiful and unique these dwarf buffaloes really are.

The evolutionary anomalies of island life are among the most spectacular phenomena in nature, yet islands contain a disproportionately higher amount of threatened and extinct biota compared to continents. I have always found the ecologically naive and fragile nature of these taxa extremely intriguing. Dwarf elephants and hippos, giant rats and shrew-like insectivores larger than a cat, short-legged bovids with stereoscopic vision, deer with bizarre antlers, etc. Both the fossil record and islands today are home to mesmerizing mammal species.

Written by:

Roberto Rozzi

Postdoc, German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig

For more information: https://twitter.com/Rozzi_Roberto | https://scholar.google.it/citations?user=ZTz5g0QAAAAJ&hl=en

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(Left) View of Monte Tuttavista, one of the major Sardinian localities yielding Quaternary fossil vertebrates ranging in age from the Early to Late Pleistocene. Bovids of the so-called ‘Nesogoral group’ were also recovered from this site and included in our study. (Centre) Roberto Rozzi at Gásadalur, Vágar, Faroe Islands.
(Right) Crystal clear waters of Caló den Rafelino, Mallorca, where remains of the earliest representative of the Myotragus lineage were found (Myotragus palomboi; Early Pliocene).