Morphological innovation, diversification and invasion of a new adaptive zone

How ecological opportunity relates to diversification is a central question in evolutionary biology. However, there are few empirical examples of how ecological opportunity and morphological innovation open new adaptive zones, and promote diversification. We analyse data on diet, skull morphology and bite performance, and relate these traits to diversification rates throughout the evolutionary history of an ecologically diverse family of mammals (Chiroptera: Phyllostomidae). We found a significant increase in diversification rate driven by increased speciation at the most recent common ancestor of the predominantly frugivorous subfamily Stenodermatinae. The evolution of diet was associated with skull morphology, and morphology was tightly coupled with biting performance, linking phenotype to new niches through performance. Following the increase in speciation rate, the rate of morphological evolution slowed, while the rate of evolution in diet increased. This pattern suggests that morphology stabilized, and niches within the new adaptive zone of frugivory were filled rapidly, after the evolution of a new cranial phenotype that resulted in a certain level of mechanical efficiency. The tree-wide speciation rate increased non linearly with a more frugivorous diet, and was highest at measures of skull morphology associated with morphological extremes, including the most derived Stenodermatines. These results show that a novel stenodermatine skull phenotype played a central role in the evolution of frugivory and increasing speciation within phyllostomids.

[1]  Kate E. Jones,et al.  The delayed rise of present-day mammals , 1990, Nature.

[2]  E. Dumont,et al.  Connecting behaviour and performance: the evolution of biting behaviour and bite performance in bats , 2009, Journal of evolutionary biology.

[3]  M. Donoghue,et al.  A Bayesian approach for evaluating the impact of historical events on rates of diversification , 2009, Proceedings of the National Academy of Sciences.

[4]  C. Darwin The Origin of Species by Means of Natural Selection, Or, The Preservation of Favoured Races in the Struggle for Life , 2019 .

[5]  Doug M. Boyer,et al.  Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals. , 2008, Journal of human evolution.

[6]  Julian L. Davis,et al.  Mechanics of bite force production and its relationship to diet in bats , 2010 .

[7]  Kazutaka Katoh,et al.  Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework , 2008, BMC Bioinformatics.

[8]  A. Grafen The phylogenetic regression. , 1989, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  A. Herrel,et al.  The implications of food hardness for diet in bats , 2003 .

[10]  Marc A. Suchard,et al.  Many-core algorithms for statistical phylogenetics , 2009, Bioinform..

[11]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[12]  T. Popowics Postcanine dental form in the mustelidae and viverridae (Carnivora: Mammalia) , 2003, Journal of morphology.

[13]  Olaf R. P. Bininda-Emonds,et al.  transAlign: using amino acids to facilitate the multiple alignment of protein-coding DNA sequences , 2005, BMC Bioinformatics.

[14]  E. Kalko,et al.  Trophic structure in a large assemblage of phyllostomid bats in Panama , 2004 .

[15]  Anthony Herrel,et al.  Built to bite: cranial design and function in the wrinkle‐faced bat , 2009 .

[16]  Jonathan B. Losos,et al.  Adaptive Radiation, Ecological Opportunity, and Evolutionary Determinism , 2010, The American Naturalist.

[17]  F J Ayala,et al.  Tempo and mode in evolution. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. Michener,et al.  Vertical stratification of Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae) revealed by stable carbon isotopes , 2011, Journal of Tropical Ecology.

[19]  Michael J. Sanderson,et al.  TESTING FOR DIFFERENT RATES OF CONTINUOUS TRAIT EVOLUTION USING LIKELIHOOD , 2006, Evolution; international journal of organic evolution.

[20]  W. Godsoe,et al.  Ecological opportunity and the origin of adaptive radiations , 2010, Journal of evolutionary biology.

[21]  J. Hunter Key innovations and the ecology of macroevolution. , 1998, Trends in ecology & evolution.

[22]  E. Dumont The effect of food hardness on feeding behaviour in frugivorous bats (Phyllostomidae): an experimental study , 1999 .

[23]  M. Pagel,et al.  Relating Traits to Diversification: A Simple Test , 2008, The American Naturalist.

[24]  Peter Aerts,et al.  Morphological and mechanical determinants of bite force in bats: do muscles matter? , 2008, Journal of Experimental Biology.

[25]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[26]  C. Darwin On the Origin of Species by Means of Natural Selection: Or, The Preservation of Favoured Races in the Struggle for Life , 2019 .

[27]  S. O’Brien,et al.  A Molecular Phylogeny for Bats Illuminates Biogeography and the Fossil Record , 2005, Science.

[28]  D. Posada,et al.  Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. , 2004, Systematic biology.

[29]  S. O’Brien,et al.  A family matter: conclusive resolution of the taxonomic position of the long-fingered bats, miniopterus. , 2007, Molecular biology and evolution.

[30]  M. Menegon,et al.  Gradual Adaptation Toward a Range-Expansion Phenotype Initiated the Global Radiation of Toads , 2010, Science.

[31]  Chad D. Brock,et al.  Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes? , 2009, BMC Evolutionary Biology.

[32]  Richard G FitzJohn,et al.  Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. , 2009, Systematic biology.

[33]  R. Michener,et al.  Specialization and Omnivory in Diverse Mammalian Assemblages , 2010 .

[34]  THE DIVERSIFICATION OF HALENIA (GENTIANACEAE): ECOLOGICAL OPPORTUNITY VERSUS KEY INNOVATION , 2003, Evolution; international journal of organic evolution.

[35]  I. Lovette,et al.  Density-dependent diversification in North American wood warblers , 2008, Proceedings of the Royal Society B: Biological Sciences.

[36]  E. Mayr Animal Species and Evolution , 1964 .

[37]  Patricia W. Freeman Macroevolution in Microchiroptera: Recoupling morphology and ecology with phylogeny , 2000 .

[38]  J. Losos,et al.  Adaptive Radiation: Contrasting Theory with Data , 2009, Science.

[39]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[40]  S. Heard,et al.  Key evolutionary innovations and their ecological mechanisms , 1995 .

[41]  Daniel L. Rabosky LASER: A Maximum Likelihood Toolkit for Detecting Temporal Shifts in Diversification Rates from Molecular Phylogenies , 2006 .

[42]  T. Price,et al.  Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. , 2009, Trends in ecology & evolution.

[43]  E. Paradis STATISTICAL ANALYSIS OF DIVERSIFICATION WITH SPECIES TRAITS , 2005, Evolution; international journal of organic evolution.

[44]  D. Schluter,et al.  The Ecology of Adaptive Radiation , 2000 .

[45]  BATS, CLOCKS, AND ROCKS: DIVERSIFICATION PATTERNS IN CHIROPTERA , 2005, Evolution; international journal of organic evolution.

[46]  R. Calsbeek,et al.  Experimentally Replicated Disruptive Selection on Performance Traits in a Caribbean Lizard , 2008, Evolution; international journal of organic evolution.

[47]  M. Plummer,et al.  CODA: convergence diagnosis and output analysis for MCMC , 2006 .

[48]  Douglas L Altshuler,et al.  Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy. , 2007, Systematic biology.

[49]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[50]  D. Rabosky,et al.  Equilibrium speciation dynamics in a model adaptive radiation of island lizards , 2010, Proceedings of the National Academy of Sciences.

[51]  David R. Anderson,et al.  Model Selection and Multimodel Inference , 2003 .

[52]  E. Kalko,et al.  Neotropical bats in the canopy: diversity, community structure, and implications for conservation , 2001, Plant Ecology.

[53]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[54]  Lance D. McBrayer,et al.  Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole-animal performance measure , 2008 .

[55]  Anthony Herrel,et al.  The effects of gape angle and bite point on bite force in bats , 2003, Journal of Experimental Biology.

[56]  R. Ree DETECTING THE HISTORICAL SIGNATURE OF KEY INNOVATIONS USING STOCHASTIC MODELS OF CHARACTER EVOLUTION AND CLADOGENESIS , 2005, Evolution; international journal of organic evolution.

[57]  Richard G FitzJohn,et al.  Quantitative traits and diversification. , 2010, Systematic biology.

[58]  W. Jungers,et al.  Shape, relative size, and size‐adjustments in morphometrics , 1995 .

[59]  J. Jernvall,et al.  The hypocone as a key innovation in mammalian evolution. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[60]  M. Pagel Inferring evolutionary processes from phylogenies , 1997 .

[61]  S. O’Brien,et al.  Nuclear gene sequences confirm an ancient link between New Zealand's short-tailed bat and South American noctilionoid bats. , 2003, Molecular Phylogenetics and Evolution.