Phylogenetics of Archerfishes (Toxotidae) and Evolution of the Toxotid Shooting Apparatus

M G Girard; M P Davis; Tan H H; D J Wedd; P Chakrabarty; W B Ludt; A P Summers; W L Smith

doi:10.1093/iob/obac013

Phylogenetics of Archerfishes (Toxotidae) and Evolution of the Toxotid Shooting Apparatus

Integr Org Biol. 2022 Mar 21;4(1):obac013. doi: 10.1093/iob/obac013. eCollection 2022.

Authors

M G Girard¹, M P Davis², Tan H H³, D J Wedd⁴, P Chakrabarty⁵, W B Ludt⁶, A P Summers⁷, W L Smith¹

Affiliations

¹ Department of Ecology and Evolutionary Biology and Biodiversity Institute, University of Kansas, Lawrence, KS 66045, USA.
² Department of Biological Sciences, St. Cloud State University, St. Cloud, MN 56301, USA.
³ Lee Kong Chian Natural History Museum, National University of Singapore, 117377, SGP.
⁴ Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT 0810, AUS.
⁵ Ichthyology Section, Museum of Natural Science, Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
⁶ Department of Ichthyology, Natural History Museum of Los Angeles County, Los Angeles, CA 90007, USA.
⁷ Department of Biology and SAFS, University of Washington's Friday Harbor Laboratories, Friday Harbor, WA 98250, USA.

Abstract

Synopsis: Archerfishes (Toxotidae) are variously found in the fresh- and brackish-water environments of Asia Pacific and are well known for their ability to shoot water at terrestrial prey. These shots of water are intended to strike their prey and cause it to fall into the water for capture and consumption. While this behavior is well known, there are competing hypotheses (blowpipe vs. pressure tank hypothesis) of how archerfishes shoot and which oral structures are involved. Current understanding of archerfish shooting structures is largely based on two species, Toxotes chatareus and T. jaculatrix. We do not know if all archerfishes possess the same oral structures to shoot water, if anatomical variation is present within these oral structures, or how these features have evolved. Additionally, there is little information on the evolution of the Toxotidae as a whole, with all previous systematic works focusing on the interrelationships of the family. We first investigate the limits of archerfish species using new and previously published genetic data. Our analyses highlight that the current taxonomy of archerfishes does not conform to the relationships we recover. Toxotes mekongensis and T. siamensis are placed in the synonymy of T. chatareus, Toxotes carpentariensis is recognized as a species and removed from the synonymy of T. chatareus, and the genus Protoxotes is recognized for T. lorentzi based on the results of our analyses. We then take an integrative approach, using a combined analysis of discrete hard- and soft-tissue morphological characters with genetic data, to construct a phylogeny of the Toxotidae. Using the resulting phylogenetic hypothesis, we then characterize the evolutionary history and anatomical variation within the archerfishes. We discuss variation in the oral structures and the evolution of the mechanism with respect to the interrelationships of archerfishes, and find that the oral structures of archerfishes support the blowpipe hypothesis but soft-tissue oral structures may also play a role in shooting. Finally, by comparing the morphology of archerfishes to their sister group, we find that the Leptobramidae has relevant shooting features in the oral cavity, suggesting that some components of the archerfish shooting mechanism are examples of co-opted or exapted traits.

Sinopsis malay: Pelbagai jenis Ikan Sumpit (Toxotidae) dapat dijumpai di persekitaran air tawar dan payau di Asia Pasifik dan mereka terkenal dengan kebolehan mereka menembak air ke arah mangsa di darat. Tembakan air ini bertujuan untuk menyerang mangsa mereka dan menyebabkan mereka jatuh ke dalam air untuk ditangkap dan dimakan. Walaupun tingkah laku ini diketahui umum, terdapat hipotesis yang bersaing (hipotesis sumpitan vs. tangki tekanan) tentang cara ikan sumpit menembak dan struktur mulut yang terlibat. Pemahaman semasa tentang struktur menembak ikan sumpit adalah sebahagian besarnya berdasarkan dua spesies, Toxotes chatareus dan T. jaculatrix. Kami tidak pasti sama ada semua ikan sumpit mempunyai struktur mulut yang sama untuk menembak air, jika variasi anatomi terdapat dalam struktur mulut ini, atau bagaimana ciri-ciri ini telah berkembang. Tambahan pula, terdapat sedikit maklumat tentang evolusi Toxotidae secara keseluruhan, dengan semua penyelidikan sistematik sebelum ini memfokuskan pada hubungan saling keluarga. Kami pada mulanya mengkaji had spesies ikan sumpit ini menggunakan data genetik baharu dan yang diterbitkan sebelum ini. Analisis kami menunjukkan bahawa taksonomi semasa ikan sumpit tidak mematuhi hubungan yang kami perolehi. Toxotes mekongensis dan T. siamensis diletakkan bersama kesinoniman T. chatareus, Toxotes carpentariensis yang diiktiraf sebagai satu spesies dan dikeluarkan daripada kesinoniman T. chatareus, dan genus Protoxotes yang diiktiraf untuk T. lorentzi adalah berdasarkan hasil analisis kami. Kemudian kami mengambil pendekatan integratif, menggunakan analisis gabungan karakter morfologi tisu keras dan lembut diskret dengan data genetik, untuk membina filogeni Toxotidae. Menggunakan hipotesis filogenetik yang terhasil, kami kemudian mencirikan sejarah evolusi dan variasi anatomi dalam ikan sumpit. Kami membincangkan variasi dalam struktur mulut dan evolusi mekanisme berkenaan yang berkaitan dengan ikan sumpit, dan mendapati bahawa struktur mulut ikan sumpit menyokong hipotesis sumpitan tetapi struktur mulut tisu lembut juga mungkin memainkan peranan dalam cara menembak. Akhir sekali, dengan membandingkan morfologi ikan sumpit kepada kumpulan saudara mereka, kami mendapati bahawa Leptobramidae mempunyai ciri penangkapan yang relevan dalam rongga mulut mereka, menunjukkan bahawa beberapa komponen mekanisme penangkapan ikan sumpit merupakan contoh ciri-ciri yang diikut-sertakan atau diguna semula.