Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae)

Spanke T., Hilgers L., Wipfler B., Flury J.M., Nolte A.W., Utama I.V., Misof B., Herder F., Schwarzer J.

Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, Bonn, 53113, Germany; Carl Von Ossietzky Universität Oldenburg, AG Ökologische Genomik, Carl von Ossietzky-Str. 9-11, Oldenburg, 26111, Germany; Ichthyology Laboratory, Indonesian Institute of Sciences (LIPI), JL. Raya Jakarta-Bogor Km. 46, Cibinong, 16911, Indonesia


Background: Pelvic brooding is a form of uni-parental care, and likely evolved in parallel in two lineages of Sulawesi ricefishes. Contrary to all other ricefishes, females of pelvic brooding species do not deposit eggs at a substrate (transfer brooding), but carry them until the fry hatches. We assume that modifications reducing the costs of egg carrying are beneficial for pelvic brooding females, but likely disadvantageous in conspecific males, which might be resolved by the evolution of sexual dimorphism via sexual antagonistic selection. Thus we hypothesize that the evolution of pelvic brooding gave rise to female-specific skeletal adaptations that are shared by both pelvic brooding lineages, but are absent in conspecific males and transfer brooding species. To tackle this, we combine 3D-imaging and morphometrics to analyze skeletal adaptations to pelvic brooding. Results: The morphology of skeletal traits correlated with sex and brooding strategy across seven ricefish species. Pelvic brooding females have short ribs caudal of the pelvic girdle forming a ventral concavity and clearly elongated and thickened pelvic fins compared to both sexes of transfer brooding species. The ventral concavity limits the body cavity volume in female pelvic brooders. Thus body volumes are smaller compared to males in pelvic brooding species, a pattern sharply contrasted by transfer brooding species. Conclusions: We showed in a comparative framework that highly similar, sexually dimorphic traits evolved in parallel in both lineages of pelvic brooding ricefish species. Key traits, present in all pelvic brooding females, were absent or much less pronounced in conspecific males and both sexes of transfer brooding species, indicating that they are non-beneficial or even maladaptive for ricefishes not providing extended care. We assume that the combination of ventral concavity and robust, elongated fins reduces drag of brooding females and provides protection and stability to the egg cluster. Thus ricefishes are one of the rare examples where environmental factors rather than sexual selection shaped the evolution of sexually dimorphic skeletal adaptations. © 2021, The Author(s).

Adrianichthys; Maternal care; Oryzias; Rib length; Ribs; Sexual antagonistic selection; Sexual dimorphism


BMC Ecology and Evolution

Publisher: BioMed Central Ltd

Volume 21, Issue 1, Art No 57, Page – , Page Count

Journal Link:

doi: 10.1186/s12862-021-01791-z

Issn: 14726785

Type: All Open Access, Gold, Green


Schluter, D., (2000) The ecology of adaptive radiation, , Oxford University Press, Oxford; Arendt, J., Reznick, D., Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? (2008) Trends Ecol Evol, 23, pp. 26-32; Bolnick, D.I., Barrett, R.D.H., Oke, K.B., Rennison, D.J., Stuart, Y.E., (Non)parallel evolution (2018) Annu Rev Ecol Evol Syst, 49, pp. 303-330; McGhee, G.R., (2011) Convergent evolution: limited forms most beautiful, , MIT Press, Cambridge, Massachusetts; Mank, J.E., Promislow, D.E.L., Avise, J.C., Phylogenetic perspectives in the evolution of parental care in ray-finned fishes (2005) Evolution, 59, pp. 1570-1578; Reznick, D.N., Mateos, M., Springer, M.S., Independent origins and rapid evolution of the placenta in the fish genus poeciliopsis (2002) Science, 298, pp. 1018-1020; Emlen, S.T., Oring, L.W., Ecology, sexual selection, and the evolution of mating systems (1977) Science, 197, pp. 215-223. , COI: 1:STN:280:DyaE2s3hsFyrtQ%3D%3D; Clutton-Brock, T.H., (1991) The evolution of parental care, , Princeton University Press, Princeton, New Jersey; Andersson, M., (1994) Sexual selection, , Princeton University Press, Princeton; Lessells, C.M., Sexual conflict (2012) The evolution of parental care, pp. 150-170. , Royle NJ, Smiseth PT, Kölliker M, (eds), Oxford University Press, Oxford; Slatkin, M., Ecological causes of sexual dimorphism (1984) Evolution, 38, pp. 622-630; Gross, M.R., Sargent, R.C., The evolution of male and female parental care in fishes (1985) Integr Comp Biol, 25, pp. 807-822; Forstmeier, W., Leisler, B., Kempenaers, B., Bill morphology reflects female independence from male parental help (2001) Proc R Soc London Ser B Biol Sci, 268, pp. 1583-1588; Samuk, K., Iritani, D., Schluter, D., Reversed brain size sexual dimorphism accompanies loss of parental care in white sticklebacks (2014) Ecol Evol, 4, pp. 3236-3243; Ronco, F., Roesti, M., Salzburger, W., A functional trade-off between trophic adaptation and parental care predicts sexual dimorphism in cichlid fish (2019) Proc R Soc B Biol Sci, 286, p. 20191050; Balon, E.K., Reproductive guilds of fishes: a proposal and definition (1975) J Fish Res Board Canada, 32, pp. 821-864; Balon, E.K., About processes which cause the evolution of guilds and species (1981) Environ Biol Fishes, 6, pp. 129-138; Royle, N.J., Smiseth, P.T., Kölliker, M., (2012) The evolution of parental care, , Oxford University Press, Oxford; Ripley, J.L., Foran, C.M., Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.) (2009) J Comp Physiol B., 179, pp. 325-333; Wilson, A.B., Male pregnancy in seahorses and pipefishes (Family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny (2001) J Hered, 92, pp. 159-166; Monteiro, N., Almada, V., Vieira, M., Implications of different brood pouch structures in syngnathid reproduction (2005) J Mar Biol Assoc UK, 85, pp. 1235-1241; Mokodongan, D.F., Yamahira, K., Origin and intra-island diversification of Sulawesi endemic Adrianichthyidae (2015) Mol Phylogenet Evol, 93, pp. 150-160; Parenti, L.R., A phylogenetic analysis and taxonomic revision of ricefishes, Oryzias and relatives (Beloniformes, Adrianichthyidae) (2008) Zool J Linn Soc, 154, pp. 494-610; Herder, F., Hadiaty, R.K., Nolte, A.W., Pelvic-Fin brooding in a new species of riverine ricefish (Atherinomorpha: Beloniformes: Adrianichthyidae) from Tana Toraja, Central Sulawesi (2012) Indonesia Raffles Bull Zool, 60, pp. 467-476; Yamamoto, T., (1975) Medaka: (Killifish). Biology and strains. Series of stock culture in biological field, , Keigaku Publishing Company, Tokyo; Wootton, R.J., Smith, C., (2014) Reproductive biology of teleost fishes, , Wiley, Chichester; Iwamatsu, T., Kobayashi, H., Shibata, Y., Sato, M., Tsuji, N., Takakura, K., Oviposition cycle in the oviparous fish Xenopoecilus sarasinorum (2007) Zool Sci, 24, pp. 1122-1127; Kottelat, M., Synopsis of the endangered Buntingi (Osteichthyes: Adrianichthyidae and Oryziidae) of Lake Poso, Central Sulawesi, Indonesia, with a new reproductive guild and descriptions of three new species (1990) Ichthyol Explor Freshwaters, 1, pp. 49-67; Iwamatsu, T., Kobayashi, H., Sato, M., Yamashita, M., Reproductive role of attaching filaments on the egg envelope in Xenopoecilus sarasinorum (Adrianichthidae, Teleostei) (2008) J Morphol, 269, pp. 745-750; Parenti, L.R.L., The phylogeny of Atherinomorphs: evolution of a novel fish reproductive system (2005) Viviparous fishes, pp. 13-30. , Uribe M, Grier HJ, (eds), New Life Press, Homestead; Popta, C.M.L., Haplochilus sarasinorum, n. sp (1905) Notes from Leyden Museum, 25, pp. 239-247; Weber, M., de Beaufort, L.F., (1922) The Fishes of the Indo-Australian Archipelago: Heteromi, Solenichthyes, Synentognathi, Percesoces, Labyrinthici, Microcyprini, , EJ Brill Limited, Leiden; Mokodongan, D.F., Tanaka, R., Yamahira, K., A New Ricefish of the Genus Oryzias (Beloniformes, Adrianichthyidae) from Lake Tiu, Central Sulawesi (2014) Indonesia Copeia, 2014, pp. 561-567; Mandagi, I.F., Mokodongan, D.F., Tanaka, R., Yamahira, K., A New Riverine Ricefish of the Genus Oryzias (Beloniformes, Adrianichthyidae) from Malili, Central Sulawesi (2018) Indonesia Copeia, 106, pp. 297-304; Cooke, S.J., Philipp, D.P., Wahl, D.H., Weatherhead, P.J., Energetics of parental care in six syntopic centrarchid fishes (2006) Oecologia, 148, pp. 235-249; Alonso-Alvarez, C., Velando, A., Benefits and costs of parental care (2012) The evolution of parental care, pp. 40-61. , Royle PN, Smiseth P, Kölliker M, (eds), Oxford University Press, Oxford; Gallesi, M.M., Mobili, S., Cigognini, R., Hardersen, S., Sacchi, R., Sexual dimorphism in wings and wing bands of Sympetrum pedemontanum (Müller in Allioni 1776) (2015) Zoomorphology, 134, pp. 531-540; Temeles, E.J., Pan, I.L., Brennan, J.L., Horwitt, J.N., Evidence for ecological causation of sexual dimorphism in a hummingbird (2000) Science, 289, pp. 441-443; Carter, H.J., Musick, J.A., Sexual dimorphism in the deep-sea fish Barathrodemus manatinus (Ophidiidae) (1985) Copeia, 1985, pp. 69-73; Britz, R., Conway, K.W., Osteology of Paedocypris, a miniature and highly developmentally truncated fish (Teleostei: Ostariophysi: Cyprinidae) (2009) J Morphol, 270, pp. 389-412; Yamanoue, Y., Setiamarga, D.H.E., Matsuura, K., Pelvic fins in teleosts: structure, function and evolution (2010) J Fish Biol, 77, pp. 1173-1208; Harris, J.E., The role of the fins in the equilibrium of the swimming fish (1936) J Exp Biol, 13, pp. 476-493; Gosline, W.A., (1971) Functional morphology and classification of teleostean fishes, , University Press of Hawaii, Honolulu; Lahti, D.C., Johnson, N.A., Ajie, B.C., Otto, S.P., Hendry, A.P., Blumstein, D.T., Relaxed selection in the wild (2009) Trends Ecol Evol, 24, pp. 487-496; Nachtigall, W., (1974) Biological mechanisms of attachment, , Springer, Berlin; Davenport, J., How and why do flying fish fly? (1994) Rev Fish Biol Fish, 4, pp. 184-214; Wetzel, J., Wourms, J.P., Adaptations for reproduction and development in the skin-brooding ghost pipefishes (1995) Solenostomus Environ Biol Fishes, 44, pp. 363-384; Regan, C.T., Phallostethus dunckeri, a remarkable new Cyprinodont fish from Johore (1913) Ann Mag Nat Hist, 12, pp. 548-555; Parenti, L.R., Homology of pelvic fin structures in female Phallostethid Fishes (Atherinomorpha, Phallostethidae) (1986) Copeia, 1986, p. 305; Gundo, M.T., Rahardjo, M.F., Hadie, W., Dimorfisme seksual dan mikroanatomi ovarium ikan endemik rono (Adrianichthys oophorus, Kottelat 1990) di Danau Poso Sulawesi Tengah [Sexual dimorphism and ovarian microanatomy of the endemic eggcarrying buntingi Adrianichthys oophorus, Kottelat 1990] (2013) J Iktiologi Indones, 13, pp. 55-65; Kottelat, M., The ricefishes (Oryziidae) of the Malili Lakes, Sulawesi, Indonesia, with description of a new species (1990) Ichthyol Explor Freshw, 1, pp. 151-166; Herder, F., Chapuis, S., Oryzias hadiatyae, a new species of ricefish (Atherinomorpha: Beloniformes: Adrianichthyidae) endemic to Lake Masapi, Central Sulawesi (2010) Indonesia Raffles Bull Zool, 58, pp. 269-280; Parenti, L.R., Hadiaty, R.K., Lumbantobing, D., Herder, F., Two New Ricefishes of the Genus Oryzias (Atherinomorpha: Beloniformes: Adrianichthyidae) augment the endemic freshwater fish fauna of Southeastern Sulawesi (2013) Indonesia Copeia, 2013, pp. 403-414; Mundry, R., Statistical issues and assumptions of phylogenetic generalized least squares (2014) Modern phylogenetic comparative methods and their application in evolutionary biology, pp. 131-153. , Garamszegi LZ, (ed), Springer, Berlin; Montgomerie, R.D., Weatherhead, P.J., Risks and rewards of nest defence by parent birds (1988) Q Rev Biol, 63, pp. 167-187; Magnhagen, C., Parental care and predation risk in fish (1992) Ann Zool Fennici, 29, pp. 227-232; Townsend, D.S., The costs of male parental care and its evolution in a neotropical frog (1986) Behav Ecol Sociobiol, 19, pp. 187-195; Smith, C., Wootton, R.J., The costs of parental care in teleost fishes (1995) Rev Fish Biol Fish, 5, pp. 7-22; Bonduriansky, R., Chenoweth, S.F., Intralocus sexual conflict (2009) Trends Ecol Evol, 24, pp. 280-288; Moore, A.J., The evolution of sexual dimorphism by sexual selection: the separate effects of intrasexual selection and intersexual selection (1990) Evolution, 44, p. 315; Fujimoto, S., Kawajiri, M., Kitano, J., Yamahira, K., Female mate preference for longer fins in Medaka (2014) Zool Sci, 31, pp. 703-708; Grant, J.W.A., Casey, P.C., Bryant, M.J., Shahsavarani, A., Mate choice by male Japanese medaka (Pisces, Oryziidae) (1995) Anim Behav, 50, pp. 1425-1428; de Camargo, N.F., de Oliveira, H.F.M., Sexual Dimorphism in Sturnira lilium (Chiroptera, Phyllostomidae): can pregnancy and pup carrying be responsible for differences in wing shape? (2012) PLoS ONE, 7; Shine, R., Keogh, S., Doughty, P., Giragossyan, H., Costs of reproduction and the evolution of sexual dimorphism in a “flying lizard” Draco melanopogon (Agamidae) (1998) J Zool, 246, pp. 203-213; Kaliontzopoulou, A., Carretero, M.A., Llorente, G.A., Intraspecific ecomorphological variation: linear and geometric morphometrics reveal habitat-related patterns within Podarcis bocagei wall lizards (2010) J Evol Biol, 23, pp. 1234-1244; Morris, J.S., Rogers, N., Rogers, A.R., Carrier, D.R., Sexual dimorphism in skeletal shape in voles (Arvicolinae): disparate selection on male bodies and female heads (2020) J Mammal, 101, pp. 951-957; Hendry, A.P., Kelly, M.L., Kinnison, M.T., Reznick, D.N., Parallel evolution of the sexes? Effects of predation and habitat features on the size and shape of wild guppies (2006) J Evol Biol, 19, pp. 741-754; Welsh, D.P., Zhou, M., Mussmann, S.M., Fields, L.G., Thomas, C.L., Pearish, S.P., The effects of age, sex, and habitat on body size and shape of the blackstripe topminnow, Fundulus notatus (Cyprinodontiformes: Fundulidae) (Rafinesque 1820) (2013) Biol J Linn Soc, 108, pp. 784-789; Foster, K., Bower, L., Piller, K., Getting in shape: habitat-based morphological divergence for two sympatric fishes (2015) Biol J Linn Soc, 114, pp. 152-162; Hayward, A., Gillooly, J.F., The cost of sex: quantifying energetic investment in gamete production by males and females (2011) PLoS ONE, 6; Baerends, G.P., Baerends-van Roon, J.M., An introduction to the study of the ethology of the cichlid fishes (1950) Behav Suppl, 1, pp. 1-243; Shaw, E.S., Aronson, L.R., Oral incubation in Tilapia macrocephala. 1, Embryological studies (1954) Bull Am Museum Nat Hist., 103, pp. 375-416; Hilgers, L., Schwarzer, J., The natural history of model organisms: the untapped potential of medaka and its wild relatives (2019) Elife, 8; Limaye, A., Drishti: A volume exploration and presentation tool (2012) Proc SPIE 8506, Dev X-Ray Tomogr VIII, ,, 85060X, 85060X; Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Fiji: an open-source platform for biological-image analysis (2012) Nat Methods, 9, pp. 676-682; Barr, D.J., Levy, R., Scheepers, C., Tily, H.J., Random effects structure for confirmatory hypothesis testing: keep it maximal (2013) J Mem Lang, 68, pp. 255-278; Kuznetsova, A., Brockhoff, P.B., Christensen, R.H.B., lmerTest package: tests in linear mixed effects models (2017) J Stat Softw, 82, pp. 1-26; Makowski, D., Ben-Shachar, M.S., Chen, S.H.A., Lüdecke, D., Indices of effect existence and significance in the Bayesian Framework (2019) Front Psychol, 10, p. 2767; Mokodongan, D.F., Yamahira, K., Mitochondrial and nuclear phylogenetic trees and divergence time estimations of Sulawesi endemic Adrianichthyidae (2015) Data Br, 5, pp. 281-284; Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., (2012) The Caper Package: Comparative Analysis of Phylogenetics and Evolution in R, ,; Paradis, E., Claude, J., Strimmer, K., APE: Analyses of phylogenetics and evolution in R language (2004) Bioinformatics, 20, pp. 289-290; Pagel, M., Inferring evolutionary processes from phylogenies (1997) Zool Scr, 26, pp. 331-348

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