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Brachymeles Evolution

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Re-evolution in the Brachymeles Genus

Introduction to Brachymeles In the lizard family Scincidae, Brachymeles is one of four genera (others being Chalcides, Lerista, and Scelotes) that contains both fully limbed and limbless species (Lande, 1978). Of the forty-one species within Brachymeles, seventeen are limbed and pentadactyl, six are externally limbless, and eighteen are neither pendactyl nor limbless (Wagner et al. 2018). The non-pentadactyl, limbed species exhibit a wide range of limb reduction and digit number. For example, B. bonitae has tiny limbs that lack complete digits, whereas B. tridactylus has moderately developed limbs, each with 3 clawed digits (Andrade et al. 2016). The Brachymeles genus and its limb traits serve as an uncommon exception to Dollo’s law of irreversibility: Once a complex trait has been lost in evolution, it cannot be regained (Gould 1970). It’s phylogenetically supported that the most recent ancestor of all Brachymeles species was likely limb and digit reduced (not to be confused with fully limbless), but the pentadactyl clade exists today with full limbs and high digit count, suggesting that they re-acquired these complex traits (Wagner et al. 2018). Statistical phylogenetics provides evidence for several instances of digit re-evolution in both the hand and foot within the brachymeles lineage, with strong support for the re-evolution of a pentadactyl hand from a digit‐reduced ancestor (Siler and Brown 2011).

Mobility & Climate Selected for Different Limb States The fossorial hypothesis states that snake-like (elongated and limb reduced) forms are adapted to burrowing, whereas quadrupeds (those that move on four limbs) have an advantage in surface locomotion. However, recent locomotive analysis indicates another conclusion: Pentadactyl brachymeles are better suited than their limb reduced counterparts at both surface locomotion and burrowing (Bergmann et al. 2020). Digging with strong forelimbs is faster and exerts less energy than burrowing snout-first, which is particularly advantageous in wet (more resistant) substrates. However, snake-like brachymeles were found to be better at initiating burrowing, especially in fine, dry substrates (Bergmann et al. 2020). This initial speed may be crucial in predator evasion. Most snake-like skinks are burrowing and live in environments with loose, dry substates. This all suggests that wet substrates pose different selective pressure on fossorial species than dry substrates; While wet substrates favor pentadactyl species, limb-reduced species hold an advantage in dry substrates.

Fig 1. Timed Phylogenetic Tree shows inferred ancestral digit state reconstructions of Brachymeles Genus. Pie charts over nodes indicate probable digit states of an ancestor. Major clades are lettered A-F; A is the crown group of Brachymeles; B is Brachymeles of the Phillipines and Thailand; C is Brachymeles of the Phillipines; D is the pentadactyl clade and its limb-reduced sister group; E is the pentadactyl clade; F is the limb and digit reduced clade. Figure reprinted from Wagner et al. (2018).

Ancestral state reconstructions support that Brachymeles most likely evolved as an elongated, limb reduced (not necessarily limbless) species 62 ± 15 Ma (Bergmann et al. 2020). At this time, the Philippines had not yet split from Asia, placing Brachymeles’ origin on the mainland of Southeast Asia. Paleoclimate research suggests that this ancestral homeland had a dry climate and looser substrates. Reduced limb species and their slithering locomotion were selected by this environment. When islands of the Philippines were splitting from the Sunda Shelf 31 ± 6 Ma, some Brachymeles populations were on board those islands while others were left behind on the mainland. As visualized in Fig 1, The mainland populations eventually became the modern, legless species of miriamae and apus, the only two Brachymeles species not endemic to the Philippines. The dry conditions of the Philippines persisted until 25 Ma, when monsoons created a far wetter climate. The soil became damp, compact, and heavily vegetated. At this time, Brachymeles diverged into two clades: limb/digit reduced and pentadactyl. The robust bodies and strong limbs of the pentadactyl clade allowed them to efficiently burrow in the moist, dense soil of their new climate. How did members of the limb reduced clade survive without locomotive advantage? The behavior of limbless reduced Brachymeles differs from that of their legged relatives. Whereas limbed Brachymeles are more surface dwelling, their limb reduced relatives are more elusive, slow-moving, and fossorial. They live burrowed in leaf litter, feeding exclusively on fossorial arthropods and hiding from surface predators.

Multiple Origins of Limb Traits The evolution of body elongation and limb reduction isn’t uncommon in vertebrate history. In squamates (snakes and lizards) alone, snake-like forms have evolved convergently at least twenty-five times (Bergmann et al. 2020). Within the Brachymeles genus alone, five separate origins of limb reduction, three of complete limb loss, and six of digit re-aquisition have been identified and supported by genetic and morphological analysis (Siler and Brown 2011). The number of origins of a phenotypic trait is largely controlled by geography and competitive interaction (Bergmann et al. 2020). If geographically separated environments have similar selection, multiple species can independently evolve the same trait. As for competitive interactions, if an adaptive niche related to a trait is already held by one or more species, that trait is less likely to become prevalent in another species. The interactions between geography and competition can also influence origins of a trait. For example, if a trait evolves in a geographically isolated species, they don’t act as competition to outside species attempting to fill the same niche. However, if that species was geographically widespread, their competitive interactions prevent more species from filling the same niche, limiting additional origins of the trait.

Fig 2. Predicted Ancestral Islands and Migrations of Brachymeles Species. Triangles indicate unambiguous ancestral area reconstructions, circles indicate ambiguous ancestral area reconstructions. Clades of focus are lettered A-C, with letters placed at the last common ancestor defining that clade. Figure reprinted from Siler et al. (2011). The Brachymeles genus is allopatric, the genus is distributed across different islands of the philippines. The numerous distinct origins of leglessness and leg reduction within the Brachymeles genus can be partially attributed to the geographical separation of its species. However, not all brachymeles species that belong to the same phylogenetic clade (typically sharing their most recent origin of limb trait) are located on the same island. This is due to dispersal events that occurred after a clade’s primary limb trait origin. Phylogenetic and geographical statistics supports five dispersal events from ancestral islands: Luzon to Mindoro, Luzon to the Visayan islands, Visayas to Mindoro, Visayas to Luzon, and the Mindanao islands to southern Luzon (Siler et al. 2011). For example, Clade C (pentadactyl with a limb-reduced sister group) of Fig 2 originated in Mindanao, but some species are found today in Luzon. In some cases, a population had another limb trait origin event after migration, explaining various limb traits and locations in one clade. The limb-reduced sister species within Clade C, B. Elerae and B. Muntingkamay, share a common ancestor that migrated from Mindanao to Luzon. After geographically separating from other members of Clade C, this lineage experienced limb reduction, a new origin of the trait, and speciated into the two limb-reduced species we know today.

Bibliography

Andrade, J.B., Lewis, R.P. and Senter, P. (2016) ‘Appendicular skeletons of five Asian skink species of the genera Brachymeles and Ophiomorus, including species with vestigial appendicular structures’, Amphibia-Reptilia, 37(4), pp. 337–344. Available at: https://doi.org/10.1163/15685381-00003062.

Bergmann, P.J. et al. (2020) ‘Locomotion and palaeoclimate explain the re-evolution of quadrupedal body form in Brachymeles lizards’, Proceedings of the Royal Society B: Biological Sciences, 287(1938), p. 20201994. Available at: https://doi.org/10.1098/rspb.2020.1994.

Gould, S.J. (1970) ‘Dollo on Dollo’s law: Irreversibility and the status of evolutionary laws’, Journal of the History of Biology, 3(2), pp. 189–212. Available at: https://doi.org/10.1007/BF00137351.

Lande R. EVOLUTIONARY MECHANISMS OF LIMB LOSS IN TETRAPODS. Evolution. 1978 Mar;32(1):73-92. doi: 10.1111/j.1558-5646.1978.tb01099.x. PMID: 28564089.

Siler, C.D. and Brown, R.M. (2011) ‘EVIDENCE FOR REPEATED ACQUISITION AND LOSS OF COMPLEX BODY-FORM CHARACTERS IN AN INSULAR CLADE OF SOUTHEAST ASIAN SEMI-FOSSORIAL SKINKS: EVOLUTIONARY SIMPLIFICATION AND REACQUISITION OF COMPLEX BODY FORM IN SKINKS’, Evolution, 65(9), pp. 2641–2663. Available at: https://doi.org/10.1111/j.1558-5646.2011.01315.x.

Siler, C.D. et al. (2011) ‘Phylogeny of Philippine slender skinks (Scincidae: Brachymeles) reveals underestimated species diversity, complex biogeographical relationships, and cryptic patterns of lineage diversification’, Molecular Phylogenetics and Evolution, 59(1), pp. 53–65. Available at: https://doi.org/10.1016/j.ympev.2010.12.019.

Wagner, G.P. et al. (2018) ‘Are there general laws for digit evolution in squamates? The loss and re‐evolution of digits in a clade of fossorial lizards ( Brachymeles , Scincinae)’, Journal of Morphology, 279(8), pp. 1104–1119. Available at: https://doi.org/10.1002/jmor.20834.


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