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The loach genus Lepidocephalichthys (Teleostei: Cobitidae) in Sri Lanka and peninsular India: multiple colonizations and unexpected species diversity

July 2023
Hydrobiologia 851(5)

DOI:10.1007/s10750-023-05321-4

Authors:

Hiranya Sudasinghe

Universität Bern

Neelesh Dahanukar

Shiv Nadar University

Rajeev Raghavan

Kerala University of Fisheries and Ocean studies

Tharindu Ranasinghe

Wild Island Foundation

Show all 8 authorsHide

Loaches of the genus Lepidocephalich-thys are ubiquitous in Peninsular India and the nearby continental-shelf island of Sri Lanka. Four valid species are reported from this region: L. thermalis, a species reported from across this region; L. jonk-laasi, confined to rainforests in southern Sri Lanka; L. coromandelensis, from the Eastern Ghats and L. guntea, from the northern Western Ghats of the Indian peninsula. Here, based on collections from 25 locations in 13 river basins in Sri Lanka and 20 locations across India, including a dataset downloaded from GenBank, we present a molecular phylogeny constructed from the mitochondrial cytochrome b (cytb) and cytochrome c oxidase subunit 1 (cox1) sequences. We show that ancestral Lepidocephalich-thys colonized Sri Lanka in the late Miocene. Multiple back-migrations to India, as well as colonizations from the mainland, took place in the Plio-Pleisto-cene. The persistence on the island of L. jonklaasi, an obligatory rainforest associate, suggests that per-humid refugia existed in Sri Lanka throughout this Handling editor: Louise Chavarie Supplementary Information The online version contains supplementary material available at https:// doi. time. Lepidocephalichthys thermalis appears to have colonized the Sri Lankan highlands as recently as the Pleistocene. The data suggest that Lepidocephalich-thys thermalis is a species complex in which multiple species remain to be investigated and described, both in India and Sri Lanka.

Molecular phylogenetic relationships of Lepidocephalichthys based on Maximum likelihood inference of the concatenated mitochondrial (cytb + cox1, 1719 bp) dataset for 280 samples. Node support (shown above the node) represents ultrafast bootstrapping for 1,000 iterations. Node support below 70 is not labeled. Scale bar represents number of changes per site. Color bars to the right of taxon labels indicate geographic distribution. The alternating grey and black bars indicate the results of the mPTP and ASAP molecular species delimitation analyses

…

a Molecular phylogenetic relationships of Lepidocephalichthys, with a focus on b the Thermalis clade, based on Maximum likelihood inference of the concatenated mitochondrial (1,719 bp) dataset of 280 samples. Node support shown above represents ultrafast bootstrapping for 1,000 iterations. Node support below 70 is not labeled. Subclades in the Thermalis clade are labelled numerically. Symbols to the right of subclades indicate the geographic distribution in the d map. Numbers in parentheses represent the sampling localities listed in Tables 1 and S1. The alternating grey and black bars indicate the results of the mPTP and ASAP molecular species delimitation analyses. Previously misidentified species of Lepidocephalichthys are indicated by an asterisk. c Bayesian time-calibrated tree of the Thermalis clade, based on the concatenated mitochondrial (1,719 bp) dataset. Bars and values at nodes represent 95% HPD and mean ages of divergence estimates, respectively

…

a Geographical origin of samples of Lepidocephalichthys jonklaasi used in the molecular analysis. Numbers on the map represent the sampling localities listed in Table 1. Median-joining haplotype networks for L. jonklaasi, based on the analysis of b a 630 bp fragment of the cox1 gene, and c a 1,089 bp fragment of the cytb gene. The number of mutational steps > 1 is shown. Legend colors correspond to river basins. The 50 m isobath (dark blue) is that derived by GEBCO Compilation Group (2020). Major river basins in Sri Lanka are labelled in black

…

a Geographical origin of samples of Lepidocephalichthys thermalis (L6) and L. cf. thermalis (L5) used in the molecular analysis. Numbers on the map represent the sampling localities listed in Tables 1 and S1. Median-joining haplotype networks for L. thermalis and L. cf. thermalis, based on the analysis of b a 630 bp fragment of the cox1 gene, and c a 1,089 bp fragment of the cytb gene. The number of mutational steps > 1 is shown. Legend colors correspond to river basins. The 50 m isobath (dark blue) is that derived by GEBCO Compilation Group (2020)

…

PCA biplot of factor scores and factor loadings for measurements of Sri Lankan Lepidocephalichthys. Ellipses delineate 95% confidence intervals

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Hydrobiologia (2024) 851:1113–1133

https://doi.org/10.1007/s10750-023-05321-4

PRIMARY RESEARCH PAPER

The loach genus Lepidocephalichthys (Teleostei: Cobitidae)

inSri Lanka andpeninsular India: multiple colonizations

andunexpected species diversity

HiranyaSudasinghe· NeeleshDahanukar· RajeevRaghavan· TharinduRanasinghe·

KumuduWijesooriya· RohanPethiyagoda· LukasRüber· MadhavaMeegaskumbura

Received: 4 May 2023 / Revised: 26 June 2023 / Accepted: 8 July 2023 / Published online: 21 July 2023

Abstract Loaches of the genus Lepidocephalich-

thys are ubiquitous in Peninsular India and the nearby

continental-shelf island of Sri Lanka. Four valid

species are reported from this region: L. thermalis,

a species reported from across this region; L. jonk-

laasi, conﬁned to rainforests in southern Sri Lanka;

L. coromandelensis, from the Eastern Ghats and

L. guntea, from the northern Western Ghats of the

Indian peninsula. Here, based on collections from 25

locations in 13 river basins in Sri Lanka and 20 loca-

tions across India, including a dataset downloaded

from GenBank, we present a molecular phylogeny

constructed from the mitochondrial cytochrome b

(cytb) and cytochrome c oxidase subunit 1 (cox1)

sequences. We show that ancestral Lepidocephalich-

thys colonized Sri Lanka in the late Miocene. Multi-

ple back-migrations to India, as well as colonizations

from the mainland, took place in the Plio-Pleisto-

cene. The persistence on the island of L. jonklaasi,

an obligatory rainforest associate, suggests that per-

humid refugia existed in Sri Lanka throughout this

Handling editor: Louise Chavarie

Supplementary Information The online version

contains supplementary material available at https:// doi.

org/ 10. 1007/ s10750- 023- 05321-4.

H.Sudasinghe

Evolutionary Ecology andSystematics Laboratory,

Department ofMolecular Biology andBiotechnology,

University ofPeradeniya, Peradeniya20400, SriLanka

H.Sudasinghe

Postgraduate Institute ofScience, University

ofPeradeniya, Peradeniya20400, SriLanka

H.Sudasinghe

Evolutionary Ecology, Institute ofEcology andEvolution,

University ofBern, 3012Bern, Switzerland

H.Sudasinghe· L.Rüber

Naturhistorisches Museum Bern, Bernastrasse, 15,

3005Bern, Switzerland

N.Dahanukar

Department ofLife Sciences, School ofNatural Sciences,

Shiv Nadar Institution ofEminence, Delhi-NCR,

GreaterNoida, India

R.Raghavan

Department ofFisheries Resource Management, Kerala

University ofFisheries andOcean Studies (KUFOS),

Kochi, India

T.Ranasinghe

Wild Island Foundation, 6A, Mendis Lane,

Moratuwa10400, SriLanka

K.Wijesooriya

Department ofZoology, Faculty ofScience, University

ofPeradeniya, Peradeniya20400, SriLanka

R.Pethiyagoda

Ichthyology Section, Australian Museum, Sydney, NSW,

Australia

L.Rüber

Aquatic Ecology andEvolution, Institute ofEcology

andEvolution, University ofBern, 3012Bern, Switzerland

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

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July 2023

Hiranya Sudasinghe · Neelesh Dahanukar · Rajeev Raghavan · Tharindu Ranasinghe · Madhava Meegaskumbura

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Lepidocephalichthys balios, a new species of loach from central Laos (Teleostei: Cobitidae)

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RAFFLES B ZOOL

Maurice Kottelat

Lepidocephalichthys balios, new species, is described from the Nam Mang watershed, a tributary of the Mekong, in central Laos. It is a small-sized species (largest known specimen 32.6 mm SL) distinguished from all congeners (except L. eleios) in having the last two rays of the pectoral fin in the male adjacent, without membrane between them but not fused, and without dorsal flange or projections (vs. unbranched parts fused and forming a thick rigid rod, with a dorsal projection). The body is entirely covered by isolated randomly distributed pigments, at places concentred in a midlateral row of 5–10 weakly contrasted irregular blotches and 6–9 irregular saddles, and the black basal caudal pattern made of two vertically elongated blotches. The species was collected in leaf litter and in vegetation at the bottom of a pool in a slow flowing stream.

Sri Lanka's elusive freshwater spiny eel, Macrognathus pentophthalmos (Teleostei: Mastacembelidae)

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ZOOTAXA

This study focuses on Macrognathus pentophthalmos, one of the two freshwater spiny eel species in Sri Lanka, which was once abundant in lowland floodplains. However, since the 1980s, this species has experienced a significant population decline, the causes of which remain unknown. It is presently assessed as Critically Endangered in the National Red List. Here, we report on a juvenile and an adult M. pentophthalmos discovered in the dry zone lowlands of the island. Using the mitochondrial cytochrome oxidase subunit 1 marker, we reveal subtle genetic differences between M. pentophthalmos and its Indian congener, M. aral. Additionally, we delve into the historical records of M. pentophthalmos in Sri Lanka, tracing its decline, and suggest strategic hotspots for further investigation into its current status. This study aims to contribute insights into the enigmatic decline of this species while shedding light on its genetic relationships and proposing targeted areas for conservation efforts.

Biogeography and evolutionary history of Puntius sensu lato (Teleostei: Cyprinidae) in Sri Lanka

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Oct 2023

Sri Lanka's biota is derived largely from Southeast Asian lineages which immigrated via India following its early-Eocene contact with Laurasia. The island is now separated from southeastern India by the 30 km wide Palk Strait which, during sea-level low-stands, was bridged by the 140 km-wide Palk Isthmus. Consequently, biotic ingress and egress were mediated largely by the climate of the isthmus. Because of their dependence on perennial aquatic habitats, freshwater fish are useful models for biogeographic studies. Here we investigate the timing and dynamics of the colonization of-and diversification on-Sri Lanka by a group of four closely-related genera of cyprinid fishes (Puntius sensu lato). We construct a molecular phylogeny based on two mitochondrial and two nuclear gene markers, conduct divergence timing analyses and ancestral-range estimations to infer historical biogeography, and use haplotype networks to discern phylogeographic patterns. The origin of Puntius s.l. is dated to ~ 20 Ma. The source of diversification of Puntius s.l. is Sri Lanka-Peninsular India. Species confined to perhumid rainforests show strong phylogeographic structure, while habitat generalists show little or no such structure. Ancestral range estimations for Plesiopuntius bimaculatus and Puntius dorsalis support an 'Out of Sri Lanka' scenario. Sri Lankan Puntius s.l. derive from multiple migrations across the Palk Isthmus between the early Miocene and the late Pleistocene. Species dependent on an aseasonal climate survived aridification in rainforest refugia in the island's perhumid southwest and went on to recolonize the island and even southern India when pluvial conditions resumed. Our results support an historical extinction of Sri Lanka's montane aquatic fauna, followed by a recent partial recolonization of the highlands, showing also that headwater stream capture facilitated dispersal across basin boundaries.

Phylogenetic and phylogeographic insights into Sri Lankan killifishes (Teleostei: Aplocheilidae)

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May 2024
J FISH BIOL

Three nominal species of the killifish genus Aplocheilus are reported from the lowlands of Sri Lanka. Two of these, Aplocheilus dayi and Aplocheilus werneri, are considered endemic to the island, whereas Aplocheilus parvus is reported from both Sri Lanka and Peninsular India. Here, based on a collection from 28 locations in Sri Lanka, also including a dataset of Asian Aplocheilus downloaded from GenBank, we present a phylogeny constructed from the mitochondrial cytochrome b (cytb), mitochondrial cytochrome c oxidase subunit 1 (cox1), and nuclear recombination activating protein 1 (rag1), and investigate the interrelationships of the species of Aplocheilus in Sri Lanka. The endemic Sri Lankan aplocheilid clade comprising A. dayi and A. werneri is recovered as the sister group to the clade comprising A. parvus from Sri Lanka and Aplocheilus blockii from Peninsular India. The reciprocal monophyly of A. dayi and A. werneri is not supported in our molecular phylogeny. A. dayi and A. werneri display strong sexual dimorphism, but species‐level differences are subtle, explained mostly by pigmentation patterns. Their phenotypes exhibit a parapatric distribution and may represent locally adapted forms of a single species. Alternatively, the present study does not rule out the possibility that A. dayi and A. werneri may represent an incipient species pair or that they have undergone introgression or hybridization in their contact zones. We provide evidence that the Nilwala‐Gin region of southwestern Sri Lanka may have acted as a drought refugium for these fishes.

Physiography, Climate, and Historical Biogeography of Sri Lanka in Making a Biodiversity Hotspot

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Molecular phylogeny and phylogeography of the freshwater-fish genus Pethia (Teleostei: Cyprinidae) in Sri Lanka

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Full-text available

Dec 2021
BMC Ecol

Background Sri Lanka is a continental island separated from India by the Palk Strait, a shallow-shelf sea, which was emergent during periods of lowered sea level. Its biodiversity is concentrated in its perhumid south-western ‘wet zone’. The island’s freshwater fishes are dominated by the Cyprinidae, characterized by small diversifications of species derived from dispersals from India. These include five diminutive, endemic species of Pethia ( P. bandula , P. cumingii , P. melanomaculata , P. nigrofasciata , P. reval ), whose evolutionary history remains poorly understood. Here, based on comprehensive geographic sampling, we explore the phylogeny, phylogeography and morphological diversity of the genus in Sri Lanka. Results The phylogenetic analyses, based on mitochondrial and nuclear loci, recover Sri Lankan Pethia as polyphyletic. The reciprocal monophyly of P. bandula and P. nigrofasciata , and P. cumingii and P. reval , is not supported. Pethia nigrofasciata , P. cumingii , and P. reval show strong phylogeographic structure in the wet zone, compared with P. melanomaculata , which ranges across the dry and intermediate zones. Translocated populations of P. nigrofasciata and P. reval in the Central Hills likely originate from multiple sources. Morphological analyses reveal populations of P. nigrofasciata proximal to P. bandula , a narrow-range endemic, to have a mix of characters between the two species. Similarly, populations of P. cumingii in the Kalu basin possess orange fins, a state between the red-finned P. reval from Kelani to Deduru and yellow-finned P. cumingii from Bentara to Gin basins. Conclusions Polyphyly in Sri Lankan Pethia suggests two or three colonizations from mainland India. Strong phylogeographic structure in P. nigrofasciata , P. cumingii and P. reval , compared with P. melanomaculata , supports a model wherein the topographically complex wet zone harbors greater genetic diversity than the topographically uniform dry-zone. Mixed morphological characters between P. bandula and P. nigrofasciata , and P. cumingii and P. reval , and their unresolved phylogenies, may suggest recent speciation scenarios with incomplete lineage sorting, or hybridization.

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The cyprinid genus Dawkinsia comprises 13 species distributed in lowland streams and rivers in southern peninsular India and Sri Lanka. Eleven species are endemic to India, largely restricted to streams draining the Western Ghats, while one is confined to the Knuckles Hills of Sri Lanka. One species, D. filamentosa, has a wide range, straddling the island and mainland. Here, based on 135 samples representative of all 13 species, collected from 45 locations in India and 17 in Sri Lanka, we present phylogenetic and phylogeographic analyses of Dawkinsia. We use two mitochondrial markers—cytochrome b and cytochrome c oxidase subunit 1. Dawkinsia is recovered as paraphyletic with respect to Sahyadria, with strong node support. The ‘filamentosa group’ which includes both Sri Lankan and Indian taxa (D. filamentosa, D. crassa, D. rohani, D. exclamatio, D. srilankensis, D. tambraparniei, D. arulius, D. rubrotincta and D. uttara) is recovered as the sister group of Sahyadria, a genus confined to the Western Ghats. The ‘assimilis group’, which consists entirely of Indian endemics (D. assimilis, D. austellus, D. apsara and D. lepida), is recovered as the sister group of the ‘filamentosa group’ + Sahyadria. Ancestral-range estimates indicate two colonization events from India to Sri Lanka, across the Palk Isthmus. The first of these, in the Pliocene, involved the common ancestor of D. tambraparniei and D. srilankensis, while the second was of D. filamentosa in the late Pleistocene. Dawkinsia filamentosa shows little phylogeographic structure within or between Sri Lanka and India. Ancestral-range analyses suggest that neither the Palghat nor Shencottah Gaps acted as barriers to the north–south dispersal of Dawkinsia along the Western Ghats. Instead, these valleys appear to have offered lowland passages for west–east colonization by some ancestral species across the Western Ghats ridge. Despite the Palk Isthmus having been subaerial for much of the Plio-Pleistocene and serving as the only terrestrial biotic corridor connecting Sri Lanka to the Asian mainland, it appears to have served also as a climatic filter to dispersal following the aridification of south-eastern India during the Late Miocene/early Pliocene.

Island colonization by a ‘rheophilic’ fish: the phylogeography of Garra ceylonensis (Teleostei: Cyprinidae) in Sri Lanka

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Despite exhibiting multiple morphological adaptations to living in swiftly flowing water (rheophily), Garra ceylonensis is one of the most widely distributed freshwater fish in Sri Lanka. It is thus an ideal organism to reconstruct the evolutionary history of a widespread, yet morphologically specialized, freshwater fish in a tropical-island setting. We analysed the phylogenetic and phylogeographic relationships of G. ceylonensis based on two mitochondrial and one nuclear genes. G. ceylonensis is shown to be monophyletic, with a sister-group relationship to the Indian species Garra mullya. Our results suggest a single colonization of Sri Lanka by ancestral Garra, in the late Pliocene. This suggests that the Palk Isthmus, which was exposed for most of the Pleistocene, had a hydroclimate unsuited to the dispersal of fishes such as Garra. G. ceylonensis exhibits strong phylogeographic structure: six subclades are distributed as genetically distinct populations in clusters of contiguous river basins, albeit with two exceptions. Our data reveal one or more Pleistocene extirpation events, evidently driven by aridification, with relict populations subsequently re-colonizing the island. The phylogeographic structure of G. ceylonensis suggests inter-basin dispersal largely through headwater capture, likely facilitated by free-swimming post-larvae. The Peninsular-Indian species G. mullya comprises two genetically distinct parapatric clades, which may represent distinct species.

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Mar 2021
GONDWANA RES

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We describe ASAP (Assemble Species by Automatic Partitioning), a new method to build species partitions from single locus sequence alignments (i.e. barcode datasets). ASAP is efficient enough to split datasets as large 104 sequences into putative species in several minutes. Although grounded in evolutionary theory, ASAP is the implementation of a hierarchical clustering algorithm that only uses pairwise genetic distances, avoiding the computational burden of phylogenetic reconstruction. Importantly, ASAP proposes species partitions ranked by a new scoring system that uses no biological prior insight of intra‐specific diversity. ASAP is a stand‐alone program that can be used either through a graphical web‐interface or that can be downloaded and compiled for local usage. We have assessed its power along with three others programs (ABGD, PTP and GMYC) on 10 real COI barcode datasets representing various degrees of challenge (from small and easy cases to large and complicated datasets). We also used Monte‐Carlo simulations of a multi‐species coalescent framework to assess the strengths and weaknesses of ASAP and the other programs. Through these analyses, we demonstrate that ASAP has the potential to become a major tool for taxonomists as it proposes rapidly in a full graphical exploratory interface relevant species hypothesis as a first step of the integrative taxonomy process.

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As the type species of the genus Channa, the identity of the pelvic-finless snakehead Channa orientalis Bloch is important to channid systematics. Although this name has been attached to a Sri Lankan species for the past 160 years, its vaguely specified type locality, ‘India Orientali’, has long cast doubt as to its origin. Here, based on a collection across its range in the island and analysis of the cytochrome c oxidase subunit 1 (cox1) barcoding gene, we show that the Sri Lankan pelvic-finless Channa is composed of two geographically discrete lineages separated by an uncorrected pairwise cox1 genetic distance of 6.9–8.1%. The minimum genetic distance between these two lineages and other species of the Gachua group of Channa is 5.1%. Despite their genetic divergence, the two lineages exhibit remarkable morphological stasis: they are indistinguishable from each other in external morphology. We argue that the type locality of C. orientalis is south-western Sri Lanka, to which the species is endemic. Channa orientalis is distinguished from other species of Channa by the absence of pelvic fins, adult coloration in life, dorsal- and anal-fin ray counts, number of vertebrae, and scale counts.

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Jun 2020
SYST BIODIVERS

The freshwater-fish genus Laubuka contains ∼13 species distributed through the lowlands of tropical South and South-east Asia. Four of these species (Laubuka lankensis, L. varuna, L. ruhuna, and L. insularis) are reported as endemic to Sri Lanka, a remarkable datum given the island’s small size. We sampled populations of Laubuka at 56 locations in 14 of the island’s principal river basins and analysed their morphological, meristic, phylogenetic, and phylogeographic relationships using the mitochondrial genes cytochrome b and cytochrome c oxidase subunit 1 and the nuclear recombination activating protein 1. We investigated the geographic structure, and delineated species using molecular species delimitation methods and morphological analysis within the general lineage concept of species. Molecular and morphological analyses failed to identify L. ruhuna and L. insularis as distinct species; we show them to be synonyms of L. varuna and L. lankensis, respectively. Taxonomic inflation in previous literature is attributed as a result of limited sampling and negligence of size allometry. Additionally, a third, cryptic species discovered in this study is described as L. hema sp. nov. which is evidently confined to the headwaters of the Gal basin in eastern Sri Lanka. Phylogenetic and haplotype network analyses suggest phylogeographic structure within both the southwest-endemic L. varuna and the dry-zone endemic L. lankensis, but the former shows strong phylogeographic structure between adjacent basins. The Sri Lankan species of Laubuka do not form a monophyletic group: they stem from two dispersal or vicariance events, one involving the lineage that led to L. varuna in south-western Sri Lanka, and the other, of [L. lankensis + L. hema] in the dry zone. http://zoobank.org/urn:lsid:zoobank.org:pub:D2A29329-E0E7-447E-B316-81049212CCCB http://zoobank.org/urn:lsid:zoobank.org:act:920E5DC0-CEDC-4243-98C7-12CCF829CBCD

The loach genus Lepidocephalichthys (Teleostei: Cobitidae) in Sri Lanka and peninsular India: multiple colonizations and unexpected species diversity

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