Dispersal vs. vicariance: the origin of India’s extant tetrapod fauna

Given the Indian block’s ancient association with Gondwana and subsequent separation from Africa, then Madagascar, then the Seychelles, vicariance has often been invoked to explain the distribution of some of India’s extant biota that might have had Gondwanan origins. Here I review phylogenetic studies and fossil data of Indian tetrapods to ascertain the contribution of dispersal and vicariance in shaping the assemblage. Paleogene dispersal into India accounts for almost all of the tetrapod clades in India. Vicariance is invoked for three groups, all fossorial; the caecilians, the frog family Nasikabatrachidae and the blindsnake family Gerrhopilidae. This review concludes that

2 practically all of India's Late Cretaceous tetrapod fauna (of Gondwanan origin) was extirpated during the Cretaceous-Paleogene mass extinction, which may have been exacerbated by the coeval volcanism associated with the emplacement of the Deccan Trap large igneous province. Subsequently, the tetrapod fauna was built up by incoming elements as India advanced towards Asia, docking with the continent in the Paleogene.

Introduction
In the context of plate tectonics the Indian subcontinent is interesting given that most of this landmass was part of the Gondwana supercontinent through much of its geological history (Karanth 2006, Karanth 2015. The initiation of Gondwana breakup around 160 3 million years ago (Ma) and the resulting separation of the landmass constituting India and Madagascar (henceforth Indomadagascar) from Africa around 120 Ma was the earliest vicariance event experienced by Indian biota (Fig. 1a, 1b). This was followed by two later events, one due to India's separation from Madagascar around 90-85 Ma and another following the detachment of the Seychelles block around 65 Ma (Chatterjee and Scotese 1999, Briggs 2003, Ali and Aitchison 2008Fig. 1c, 1d). Subsequently India advanced north across Indian Ocean, crossing the equator before colliding with Eurasia in the Eocene (some estimates have it at around 55 Ma, others 20 million years later; Briggs 2003, Aitchison et al. 2007, Baxter et al. 2016Fig. 1e, 1f). The accretion of India with Eurasia has been suggested to have facilitated faunal exchange between these landmasses (Mani 1974). This geological history of the Indian plate forms the basis for the out-of-India hypothesis or the Biotic Ferry model (See Datta-Roy and Karanth 2009 and references therein). According to this model, following separation from Madagascar, the rafting Indian plate carried faunal and floral elements from the Southern continents (presumably Gondwanan forms) to Asia. After docking with Asia these lineages then disperse out of India. Thus, it has been postulated that the Indian biota today comprises a mixture of older Gondwanan forms plus younger elements that crossed over into India from Africa and Asia (Mani 1974). In this work, I refer to those lineages that have existed in India since before the initial breakup of Gondwana in the Early or Middle Jurassic as "Gondwanan forms" (c. 170 Ma).
Fossil records from India lend some support to India's biotic history described above.
The Upper Cretaceous assemblages include numerous taxa with Gondwanan affinities, including leptodactylid, hylid and ranoid frogs, madtsoiid and nigerophiid snakes, pelomedusoid turtles, mesosuchian crocodiles, abelisaurid dinosaurs, and 4 gondwanathere mammals (Prasad and Sahni 2009). In contrast, the Lower Eocene comprises mainly forms with Eurasian affinities such as pelobatid frogs, russellophiid snakes, parrot-like birds, bats, rodents, adapoid primates, artiodactyls, etc (Smith et al. 2016). Given this scenario, India provides an interesting setting for studying the relative contributions of dispersal and vicariance in shaping the biotic composition of this region.
In this regard, molecular data are being increasingly used to address this question (Karanth 2006, Datta-Roy and Karanth 2009, Joshi and Karanth 2011, Krosch et al. 2012, Toussaint et al. 2016, Sil et al. 2020. However, for a robust test of these two contrasting hypotheses it is imperative to reconstruct time-calibrated evolutionary trees of taxa sampled from multiple Gondwanan fragments, particularly Africa, Madagascar and India (Datta-Roy and Karanth 2009). The vicariance scenario would be supported when higher level relationships and the divergence of the corresponding nodes mirror the sequence and timing of plate separation, i.e., separation of African from Indo-Malagasy forms around 120 Ma followed by separation between Malagasy and India taxa around 90-85 Ma (See fig. 2). Alternatively, if the ingroup under consideration underwent diversification relatively recently (after 85 Ma to present) then, irrespective of the topology, vicariance can be rejected. This is because in such cases the origin of the group as a whole would be too recent for Gondwana vicariance to have played any role in their distribution. For example, the cichlid fishes that occur in all the former Gondwana fragments (except Australia) provide an interesting system to study the role of dispersal vs. vicariance in shaping their pantropical disjunction. The cichlid phylogeny is congruent with the sequence of plate separation in that the African forms are sister to a clade consisting of Indo-Malagasy forms. However, molecular 5 dating suggests that the divergence among these lineages occurred long after plate separation (Vences et al. 2001, Crottini et al. 2012. Thus, in the case of the cichlids, dispersal better explains their current distribution. Clearly, invoking vicariance based primarily on Gondwanan distribution and tree topology can be problematic. A crucial component in such studies is the integration of temporal information in dispersalvicariance analysis (Donoghue and Moore 2003). Since the synthesis by Datta-Roy and Karanth (2009), many global phylogenies of various groups have been published, thus providing an opportunity to revisit this issue.
India here refers to the Indian subregion, which has been assigned to a separate biogeographical unit by various authors (Wallace 1876, Blanford 1901, Mani 1974, Corbet and Hill 1992, Bansal and Karanth 2010, Sil et al. 2020 to highlight its unique biota and evolutionary history (Fig. 3). It constitutes the region south of the Himalayas, including peninsular and central India, and Sri Lanka, but excludes the Indus and Gangetic plains as well as the Thar desert that were formed recently after India's accretion to Asia. However, the northern boundaries of this subregion vary across these classifications. The islands of Lakshadweep, and Andaman and Nicobar archipelagos are also excluded. Lakshadweep islands are of recent oceanic origin, whereas the Andamans and the Nicobars fall in the Indo-Chinese and Sundaic subregions, respectively.
Recent global time-trees of a range of tetrapods are reviewed here to better understand the relative contributions of dispersal and vicariance, in the context of plate tectonics, in shaping the biotic composition of India. The tetrapod groups included are amphibians (anurans, caecilians and salamanders), mammals, squamates (snakes and lizards), testudines, crocodilians and birds. These global phylogenies are at different levels of 6 taxonomic hierarchy: birds and mammals are at the order level; squamates and anurans at the family level, caecilians and testudines at the generic level, and crocodilians at the species level. For each of these global phylogenies the representation from India was 100% for the corresponding taxonomic hierarchy; for example, all the orders of Indian birds were represented in the global bird phylogeny. Taxa whose crown group age predated the separation of Africa and Indomadagascar (160-120 Ma) and / or  were considered as a strong candidate for vicariance. Those that underwent diversification after 85 Ma were categorised as elements that dispersed into India (Fig. 2). Drawing upon a mixture of molecular phylogenetic studies and palaeotological reports I provide a comprehensive overview of the origins and assembly of the Indian tetrapod assemblage.

Amphibians
The crown group age of major amphibian clades, anurans, caecilians and salamanders, fall in the Triassic (250-200 Ma; Roelants et al. 2007), which predates Gondwana breakup. Thus, given their antiquity and lack of tolerance to salt water, amphibians have long been considered a poster group for testing plate tectonic mediated vicariance (Bocxlaer et al. 2006).

Anurans
Based on molecular dating of ranid frogs, Bossuyt and Milinkovitch (2001) invoked vicariance to explain the distribution of certain frog families such as Mantellidae and Rhacophoridae in Madagascar and India respectively. Their study suggested an out-of-India dispersal of many ranid lineages. Bossuyt et al. (2006) undertook a wider 7 sampling and opined that Eurasia colonization of ranids from Africa was also plausible. Bocxlaer et al. (2006) concluded that current distribution of major Old World frog lineages can be better explained by Late Cretaceous dispersal via the terrestrial connections between most adjacent Gondwanan landmasses. Thus, the latter two studies question the out-of-India scenario that was initially proposed to explain the distribution of Asian anurans. It should be noted, however, that these studies lacked a comprehensive sampling of anuran families from the Old World and were limited in terms of number of markers and fossil calibrations. In this regard, the recent paper by Feng et al. (2017) is of much interest, as it included 44 of the 55 global frog families and, importantly, all of those found in India. Their age-calibrated phylogeny based on 20 fossil calibrations suggests that most of the frog families that are endemic to India, and those distributed in Eurasia, diverged from their African and Malagasy counterparts around the Cretaceous-Paleogene (K-Pg) boundary (66 Ma). Thus, these events occurred appreciably later than the separation of Africa and Indomadagascar, and India and Madagascar. Furthermore, their biogeographical analyses indicate that eight out of the nine anuran families that are present in India have dispersed from Eurasia in the Cenozoic. The one exception is the endemic family Nasikabatrachidae, which is sister to Sooglossidae from Seychelles (Feng et al., 2017). The granitic islands of the Seychelles sit above a Gondwanan fragment that separated from peninsular India around 65 Ma and the divergence date for these two families is consistent with this geological date.
Additionally, the divergence of Nasikabatrachidae-Sooglossidae lineage from the ranoid frogs of the Old World fits with the geological time for the separation between

Caecilians
Caecilians have also been invoked as an exemplar of the out-of-India scenario given their antiquity and circumtropical distribution (see Wilkinson et al. 2002, Gower et al. 2002. Caecilians are found on all of the former Gondwanan fragments except Madagascar and Australia. The three Asian caecilian families, Indotyphlidae, Chikilidae and Ichthyophiidae, diverged from their West Gondwanan counterparts over 120 Ma (Kamei et al. 2012). Thus, these dates suggest their Gondwanan history and the role of Indomadagascar-Africa vicariance in shaping their distribution. However, it must be noted that molecular dating analysis in these studies have been based on a mitochondrial dataset (Wilkinson et al. 2002) or a combined mitochondrial and nuclear dataset in which the mitochondrial markers dominated the dataset (Kamei et al. 2012).
These dates need to be revalidated using a "nuclear only" dataset as there is often incongruence between mitochondrial and nuclear markers with respect to tree topology as well as divergence date (see Jana and Karanth 2019, and the references therein).
Additionally, the absence of caecilians from Madagascar is intriguing. It is plausible that they went extinct in Madagascar. However, it is also possible that the dates have been over estimated and caecilians dispersed onto the drifting Indian plate from Africa (as suggested by Briggs 2003). There is an increasing body of molecular data supporting such direct dispersal of amphibians and reptiles onto the drifting Indian plate from 9 Africa/Asia presumably via land bridge (Bocxlaer et al. 2006, Bansal andKaranth 2013).
It should be noted that no caecilian fossils have been reported from India.

Salamanders
Salamanders in Asia have a largely Palearctic distribution; the two species from India are from the Eastern Himalayas. This region falls outside of the Indian subregion and therefore not relevant here. Moreover, work by Zhang et al. (2008) suggest that the Asian salamandrids dispersed to eastern Asia from Europe around 29 Ma.

Mammals
Currently, only placental mammals are present in India. Three recent studies that reconstructed the global time-calibrated phylogeny of placental mammals are relevant. Tarver et al. (2016) suggest that the diversification of the placental orders took place 76-51 Ma; similarly, Liu et al. (2017) estimates fall between 75 and 55 Ma and thus straddles the K-Pg mass extinction. Upham et al. (2019) report that most of the divergence events among placental mammals have confidence limits that overlap the K-Pg. The critical issue, therefore, is that the event post-dates the India-Madagascar vicariance. Thus, the presence of some of these orders in India must have resulted from incoming dispersals. Clyde et al. (2003) stated that during the initial collision, modern orders of mammals dispersed into India rather than out of it. In this regard, Tarver et al.
(2016) stated that their results are compatible with placental diversification being driven by dispersal rather than vicariance. This idea is supported by the Indian paleontological record, which exhibits high diversity of placental mammals in the Early Eocene, during India's initial collision with Eurasia (Smith et al. 2016, Chatterjee et al. 2017).

Birds
As with mammals, the bird record also supports rapid diversification around the K-Pg transition (Jarvis et al. 2014, Claramunt and Cracraft 2015, Prum et al. 2015, Kimball et al. 2019. In these studies the root node of neoaves falls in the Late Cretaceous, 75-65 Ma. Furthermore, these studies also support a Late Cretaceous divergence between landfowls (Galliformes) and waterfowls (Anseriformes). Thus, inter-ordinal diversification among birds (excluding ratites) occurred after India-Madagascar separation. Fossil data lends additional support to this scenario. According to Feduccia (2003) even though birds evolved in the Late Jurassic (around 157 Ma) and underwent diversification through much of Cretaceous, these lineages were badly depleted during the K-Pg event and only a few morphological forms survived to evolve into the extant lineages we see today. Longrich et al. (2011) noted that there was a major extinction of archaic birds coinciding with the K-Pg boundary. Similarly, Brusatte et al. (2015), based on fossil data, concluded that most avian lineages were decimated at the end-Cretaceous extinction, alongside their close dinosaurian relatives and after this mass extinction modern birds emerged.

Crocodilia
The crocodilian genus Crocodylus is often referred to as an ancient morphologically conserved group whose circumtropical distribution was shaped by continental drift (see Oaks 2011 and reference therein). India harbours three crocodilian species,

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Crocodylus palustris and Crocodylus porosus (family Crocodylidae), and Gavialis gangeticus (family Gavialidae). The third crocodilian family, Alligatoridae, has been reported from Upper Cretaceous beds in India (Khosla and Sahni 2003). Oaks (2011) suggests that the all modern crocodilians date back to the Late Cretaceous. More importantly the diversification of Afro-Asian crocodilians began around the Paleocene-Eocene boundary (around 56 Ma), well after India and Madagascar had separated. Thus, the three species of crocodilians that are present on India dispersed to the landmass.

Squamates
The squamate reptiles represented consist of over 9700 species and are thus one of the most species-rich tetrapod groups (only the birds have comparable numbers, around 10000 species). Most molecular studies support a Late Jurassic to Early Cretaceous origin of all the major clades of squamates (see Zheng and Wiens, 2016

Geckos
Most of India's gecko diversity (seven out of eight genera) is in the family Gekkonidae.
The age of the root node of Gekkonidae varies depending on the study from 65 Ma Phelsuma. Hemidactylus species in Madagascar are mostly human commensals that have probably been introduced as they exhibit very little variation .
Phelsuma is related to Southwest African genera Rhoptropella (Austin et al. 2004) and Lygodactylus (Pyron et al. 2013). Importantly, phylogenetic and biogeographical studies undertaken thus far suggest that most Gekkonid genera in India dispersed into dispersal from Africa or geodispersal from Africa via Arabia (Raxworthy et al. 2002, Tolley et al. 2013.

Skinks
According to the recent squamate time-trees the Scincidae crown group began diversifying around 100 Ma (Zheng andWiens 2016, Simões et al. 2018). Thus, the separation of Africa and Indomadagascar is unlikely to have shaped their distributions.

Agamids
Much of agamid diversity of India is in the subfamily Draconinae, whereas subfamily Agaminae is largely distributed in the fringe areas of India and beyond. Macey et al. (2000) speculated that the Draconinae clade in Asia might be of Indian (out-of-India) or Southeast Asian (into India) origin. However, phylogenetic and biogeographic analyses undertaken by Grismer et al. (2016) suggest that multiple lineages of Draconinae dispersed into India from Eurasia during the Eocene. In agreement with molecular results agamids have been reported from early Eocene fossil deposits in Vastan, India (Rage et al. 2008).

Monitor lizards
The family Varanidae represented by genus the Varanus is distributed in Asia, Africa and Australia. Vidal et al. (2012) suggest an Asian origin of Varanidae followed by a dispersal into Africa and Australia in the Late Eocene.

Snakes
Snakes in India are represented by both the major clades of Serpentes, i.e., Alethinophidia (advanced snakes) and Scolecophidia (blindsnakes). Recent molecular studies infer a range of ages for the crown group Alethinophidia: 82 Ma (Miralles et al. 15 2018), 92 Ma (Zheng and Wiens 2016) and ~100 Ma (Hsiang et al. 2015, Harrington andReeder 2017). These dates fall within the time frame of India-Madagascar separation.
The earliest split within Alethinophidia, between Amerophidia and Afrophidia, corresponds to South America-Africa separation (Vidal et al. 2007). However, all families in Afrophidia arose post K-Pg mass extinction in the Paleogene (Burbrink et al. 2020). Among the two families of advanced snakes of Madagascar, colubrid lineages are nested within multiple clades of African colubrids (Lawson 2005, Vences 2004); similarly, Malagasy members of Boidae are sister to African species Chippindale 2006a, Reynolds et al. 2014). Given Indian and Malagasy forms are not sisters (not immediate ones, at least), and these families arose in the Paleogene, vicariance due to India-Madagascar separation can be ruled out as a possible mechanism for their current distribution. Interestingly both Colubridae and Boidae appear in the Early Eocene fossil deposits in Vastan, India (Rage et al. 2008). The authors also note an overall similarity of Vastan fauna to that of the Early Eocene of Europe. Additionally, the Early Eocene also represent a time when the Indian plate was close to Eurasia, therefore presence of these lineages in India is better explained by dispersal.
Scolecophidians constitute an ancient group of burrowing snakes that are distributed in all the Gondwanan fragments (South America, Africa, Madagascar, India and Australia; Vidal et al. 2010). The crown group scolecophidians began diversifying in the Early Cretaceous (Miralles et al. 2018) around the time when the Gondwana breakup was initiated. The phylogenetic and biogeographical study undertaken by Vidal et al. (2010) suggest a Gondwanan origin of blindsnakes with the earliest diversification overlapping with a vicariant event: the separation of Africa and Indomadagascar around 150 Ma.

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This was followed by another vicariance event that corresponds to India-Madagascar separation. The blindsnake lineage that became isolated on the Indian plate (family Gerrhopilidae) was carried by the rafting Indian plate to Asia (out-of-India). Among squamates, scolecophidians are perhaps the only example of a group with a Gondwanan history whose distribution has been shaped by multiple vicariance events.
Unfortunately, there are no records of scolecophidian fossils from India to fortify this conclusion.
Overall, the molecular studies reviewed above suggest that Indian squamate diversity was derived from Africa and Asia. Many of these dispersal events occurred after India's collision with Asia. The only Gondwanan lineage surviving in India are the blindsnakes of the family Gerrhopilidae. Thus, it appears that most of India's squamate diversity with Gondwanan history went extinct. Incidentally, squamate fossil data from North America exhibit 83% decline in species diversity and a dramatic decline in morphological diversity across the K-Pg (Longrich et al. 2012).

Testudines
Vicariance has been invoked to explain the distribution of freshwater turtles of the family Podocnemidae in South America and Madagascar (Noonan and Chippindale 2006b). However, this family is not present in India nor is there an associated fossil record. Global phylogenetic and biogeographical analyses of Testudines undertaken by Pereira et al. (2017) suggest that India's tortoise and freshwater turtles are the result of multiple dispersal events from Southeast Asia from the Eocene to the Miocene.

Discussion
India's unique geological history has motivated biogeographers to propose that its biota is composed of both ancient Gondwanan elements and more recent arrivals from Asia and Africa. A Gondwanan history for a given lineage would suggest that its distribution in the former Gondwanan fragments has been shaped by vicariance. However, the molecular data suggests that much of the tetrapod diversity of India is the result of post K-Pg mass extinction colonization (Fig. 4). There are three exceptions to this pattern: the caecilians, frog family Nasikabatrachidae and the blindsnake family Gerrhopilidae.
The out-of-India hypothesis is supported by certain caecilian and blindsnake lineages, whereas the nasikabatrachids are a Gondwanan relict. Remarkably, the earliest fossil evidence of modern frogs, agamids, and placental mammals appear abruptly in India during the Early Eocene (Chatterjee et al. 2017), long after the K-Pg mass extinction.
Thus, the molecular studies and limited fossil data suggest that dispersal better explains the distributions of modern tetrapod taxa of India. Furthermore, given the root ages of the extant tetrapod groups, vicariance can be ruled out as the possible reason for their current distributions in other Gondwanan fragments such as Madagascar and Australia.
In this regard, studies have pointed out that the extant Malagasy vertebrate fauna was largely assembled through dispersal from Africa post separation (Yoder andNowak 2006, Crottini et al. 2012). However, the above conclusion is not consistent with Late Cretaceous fossils from India that are of largely Gondwanan origin. It is plausible that the K-Pg mass extinction might have obliterated some of India's Gondwanan biota. Globally, dinosaurs, pterosaurs, marine reptiles and two-thirds of all marine life became extinct with the termination of the Cretaceous Period (Feduccia 2003). Squamates and birds also experienced similarly large depletions (Longrich et al. 2011, Longrich et al. 2012). In the case of Indian fauna two additional factors might have compounded extinction. Much of India's Gondwanan biota might have been under great climatic stress due to the rapid northward drift of the sub-continent at the time (Raven andAxelrod 1974, Mani 1974). Moreover, there was major volcanism associated with the Deccan Traps (Fig. 3) that took place in the Late Cretaceous-Early Palaeocene (Thewissen and McKenna 1992, Renne et al. 2015, Schoene et al. 2015, Sprain et al. 2019. At the beginning of the Paleogene, the Indian plate had probably lost much of the tetrapod diversity it had in the Cretaceous. Thus, as India moved northward from Gondwana to Eurasia, the faunal composition changed from Gondwanan affinity to Asian affinity as new forms washed in and later walked over (Chatterjee et al. 2017).
Does this mean that India does not harbour any animal lineages with Gondwanan history? Perhaps the right taxa are not being targeted. Notably, the three tetrapod groups of Gondwanan history discussed here are all fossorial. It has been noted that stable and predictable fossorial environments shelter species from dramatic aboveground environmental changes (see Cyriac and Kodandaramaiah 2018 and the references therein). In this regard, soil invertebrates might be a promising group to address this question. Given that soil invertebrates tend to be small and fossorial they are more likely to be shielded from extreme conditions on the surface. One such group are the centipedes, where studies have reported multiple lineages with Gondwanan history (Joshi and Karanth 2011). Overall, the bulk of the India's tetrapod diversity results from Cenozoic immigration. It would be interesting to determine if these dispersal events were transoceanic or geodispersal. Lineages that descended from the initial passengers that were present back in the Cretaceous probably had unusual life 19 modes that enabled them to survive the K-Pg extinction event, Deccan Trap volcanism and challenging environmental shifts associated with India's rapid migration through the climatic belts.  Indomadagascar (t1=120 Ma) and . Whereas in case of the vicariance scenario inferred dates for X and Y overlap with t1 and t2.