Geographic isolation facilitates the evolution of reproductive isolation and morphological divergence

Abstract

Geographic isolation is known to contribute to divergent evolution, resulting in unique phenotypes. Oftentimes morphologically distinct populations are found to be interfertile while reproductive isolation is found to exist within nominal morphological species revealing the existence of cryptic species. These disparities can be difficult to predict or explain especially when they do not reflect an inferred history of common ancestry which suggests that environmental factors affect the nature of ecological divergence. A series of laboratory experiments and observational studies were used to address what role biogeographic factors may play in the ecological divergence of Hyalella amphipods. It was found that geographic isolation plays a key role in the evolution of reproductive isolation and divergent morphology and that divergence cannot be explained by molecular genetic variation.

REFERENCES Al-Rabab'ah, M. A., & Williams, C. G. (2004). An ancient bottleneck in the Lost Pines of central Texas. Molecular Ecology, 13, 1075–1084. Baldinger, A. J. (2004). A new species of Hyalella (Crustacea: Amphipoda: Hyalellidae) from Ash Springs, Lincoln County, Nevada, USA, with a key to the species of the genus in North America and the Caribbean region. Journal of Natural History, 38, 1087–1096. Baldinger, A. J., Shepard, W. D., & Threloff, D. L. (2000). Two new species of Hyalella (Crustacea: Amphipoda: Hyalellidae) from Death Valley National Park, California, USA. Proceedings of The Biological Society of Washington, 113, 443–457. Bauza-Ribot, M. M., Juan, C., Nardi, F., Oromi, P., Pons, J., & Jaume, D. (2012). Mitogenomic phylogenetic analysis supports continental-scale vicariance in subterranean thalassoid crustaceans. Current Biology, 22, R909–R912. Bollache, L., & Cézilly, F. (2004). Sexual selection on male body size and assortative pairing in Gammarus pulex (Crustacea: Amphipoda): field surveys and laboratory experiments. Journal of Zoology, 264, 135–141. Bromham, L. (2009). Why do species vary in their rate of molecular evolution? Biology Letters, 5, 1–4. Butlin, R. K., Saura, M., Charrier, G., Jackson, B., André, C., Caballero, A., … Rolán-Alvarez, E. (2014). Parallel evolution of local adaptation and reproductive isolation in the face of gene flow. Evolution, 68, 935–949. Chao, L., & Carr, D. E. (1993). The molecular clock and the relationship between population size and generation time. Evolution, 47, 688–690. Cole, G. A., & Watkins, R. L. (1977). Hyalella montezuma, a new species (Crustacea: Amphipoda) from Montezuma Well, Arizona. Hydrobiologia, 52, 175–184. Crawford, D. M., & Tarter, D. C. (1979). Observations on the life history of the freshwater amphipod, Crangonyx forbesi (Hubrichtand Mackin), in a spring-fed cistern in West Virginia. American Midland Naturalist, 101, 320–325. Davis, M. B., & Shaw, R. G. (2001). Range shifts and adaptive responses to Quaternary climate change. Science, 292, 673–679. Dincă, V., Wiklund, C., Lukhtanov, V. A., Kodandaramaiah, U., Norén, K., Dapporto, L., … Friberg, M. (2013). Reproductive isolation and patterns of genetic differentiation in a cryptic butterfly species complex. Journal of Evolutionary Biology, 26, 2095–2106. Dionne, K., Dufresne, F., & Nozais, C. (2017). Overlapping trophic niches among co-occurring amphipods from a cryptic species complex. Freshwater Biology, 62, 1052–1062. Dionne, K., Vergilino, R., Dufresne, F., Charles, F., & Nozais, C. (2011). No evidence for temporal variation in a cryptic species community of freshwater amphipods of the Hyalella azteca species complex. Diversity, 3, 390–404. Dray, S., & Dufour, A. B. (2007). The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22, 1–20. d'Udekem d'Acoz, C., & Havermans, C. (2012). Two new Pseudorchomene species from the Southern Ocean, with phylogenetic remarks on the genus and related species (Crustacea: Amphipoda: Lysianassoidea: Lysianassidae: Tryphosinae). Unpublished data. Ellwood, B. B., & Gose, W. A. (2006). Heinrich H1 and 8200 yr BP climate events recorded in Hall's Cave, Texas. Geology, 34, 753–756. Eroukhmanoff, F., Hargeby, A., Arnberg, N. N., Hellgren, O., Bensch, S., & Svensson, E. I. (2009). Parallelism and historical contingency during rapid ecotype divergence in an isopod. Journal of Evolutionary Biology, 22, 1098–1110. Eroukhmanoff, F., Hargeby, A., & Svensson, E. I. (2009). Rapid adaptive divergence between ecotypes of an aquatic isopod inferred from F_ST–Q_ST analysis. Molecular Ecology, 18, 4912–4923. Faria, R., Renaut, S., Galindo, J., Pinho, C., Melo-Ferreira, J., Melo, M., … Butlin, R. (2014). Advances in ecological speciation: An integrative approach. Molecular Ecology, 23, 513–521. Fragata, I., Simões, P., Lopes-Cunha, M., Lima, M., Kellen, B., Bárbaro, M., … Matos, M. (2014). Laboratory selection quickly erases historical differentiation. PLoS One, 9, E96227. Garant, D., Forde, S. E., & Hendry, A. P. (2007). The multifarious effects of dispersal and gene flow on contemporary adaptation. Functional Ecology, 21, 434–443. Gebiola, M., Kelly, S. E., Hammerstein, P., Giorgini, M., & Hunter, M. S. (2016). “Darwin's corollary” and cytoplasmic incompatibility induced by cardinium may contribute to speciation in Encarsia wasps (Hymenoptera: Aphelinidae). Evolution, 70, 2447–2458. Gillespie, J. H. (2001). Is the population size of a species relevant to its evolution? Society for the Study of Evolution, 55, 2161–2169. Glazier, D. S. (2000). Is fatter fitter? Body storage and reproduction in ten populations of the freshwater amphipod Gammarus minus. Oecologia, 122, 335–345. Gonzalez, E. R., & Watling, L. (2002). Redescription of Hyalella azteca from its type locality, Vera Cruz, Mexico (Amphipoda: Hyalellidae). Journal of Crustacean Biology, 22, 173–183. Guzik, M. T., Cooper, S. J., Humphreys, W. F., Ong, S., Kawakami, T., & Austin, A. D. (2011). Evidence for population fragmentation within a subterranean aquatic habitat in the Western Australian desert. Heredity, 107, 215–230. Hall, S. A., & Penner, W. L. (2013). Stable carbon isotopes, C3–C4 vegetation, and 12,800 years of climate change in central New Mexico, USA. Palaeogeography, Palaeoclimatology, Palaeoecology, 369, 272–281. Havermans, C., Nagy, Z. T., Sonet, G., De Broyer, C., & Martin, P. (2011). DNA barcoding reveals new insights into the diversity of Antarctic species of Orchomene sensu lato (Crustacea: Amphipoda: Lysianassoidea). Census of Antarctic Marine Life: Diversity and Change in the Southern Ocean Ecosystems, 58, 230–241. Hendry, A. P., Wenburg, J. K., Bentzen, P., Volk, E. C., & Quinn, T. P. (2000). Rapid evolution of reproductive isolation in the wild: Evidence from introduced salmon. Science, 290, 516–518. Hou, Z., Fu, J., & Li, S. (2007). A molecular phylogeny of the genus Gammarus (Crustacea: Amphipoda). Molecular Phylogenetics and Evolution, 45, 596–611. Ishikawa, A., Takeuchi, N., Kusakabe, M., Kume, M., Mori, S., Takahashi, H., & Kitano, J. (2013). Speciation in ninespine stickleback: Reproductive isolation and phenotypic divergence among cryptic species of Japanese ninespine stickleback. Journal of Evolutionary Biology, 26, 1417–1430. Jeffroy, O., Brinkmann, H., Delsuc, F., & Philippe, H. (2008). Phylogenomics: The beginning of incongruence? Trends in Genetics, 22, 225–231. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., … Drummond, A. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. King, R., & Leys, R. (2014). Molecular evidence for mid-Pleistocene divergence of populations of three freshwater amphipod species (Talitroidea: Chiltoniidae) on Kangaroo Island, South Australia, with a new spring-associated genus and species. Australian Journal of Zoology, 62, 137–156. Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1873. Lanfear, R., Calcott, B., Ho, S. Y. W., & Guindon, S. (2012). PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701. Major, K., Soucek, D. J., Giordano, R., Wetzel, M. J., & Soto-Adames, F. (2013). The common ecotoxicology laboratory strain of Hyalella azteca is genetically distinct from most wild strains sampled in eastern North America. Environmental Toxicology and Chemistry, 32, 2637–2647. McGee, M. D., Neches, R. Y., & Seehausen, O. (2016). Evaluating genomic divergence and parallelism in replicate ecomorphs from young and old cichlid adaptive radiations. Molecular Ecology, 25, 260–268. McInerney, C. E., Maurice, L., Robertson, A. L., Knight, L. R., Arnscheidt, J., Venditti, C., … Hanfling, B. (2014). The ancient Britons: Groundwater fauna survived extreme climate change over tens of millions of years across NW Europe. Molecular Ecology, 23, 1153–1166. Muschick, M., Indermaur, A., & Salzburger, W. (2012). Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology, 22, 2362–2368. Nordt, L. C., Boutton, T. W., Hallmark, C. T., & Waters, M. R. (1994). Late Quaternary vegetation and climate changes in central Texas based on the isotopic composition of organic carbon. Quaternary Research, 41, 109–120. Nosil, P., Gompert, Z., Farkas, T. E., Comeault, A. A., Feder, J. L., Buerkle, C. L., & Parchman, T. L. (2012). Genomic consequences of multiple speciation processes in a stick insect. Proceedings of the Royal Society B: Biological Sciences, 279, 5058–5065. Nosil, L. C., Harmon, L. J., & Seehausen, O. (2009). Ecological explanations for (incomplete) speciation. Trends in Ecology and Evolution, 24, 145–156. Ohta, T. (1993). An examination of the generation-time effect on molecular evolution. Proceedings of the National Academy of Science USA, 90, 10676–10680. Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., … Wagner, H. (2016). vegan: Community ecology package. R package version 2.4-1. https://CRAN.R-project.org/package=vegan Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290. Paterson, I. D., Mangan, R., Downie, D. A., Coetzee, J. A., Hill, M. P., Burke, A. M., … Compton, S. G. (2016). Two in one: Cryptic species discovered in biological control agent populations using molecular data and crossbreeding experiments. Ecology and Evolution, 6, 6139–6150. R Development Core Team (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3-900051-07-0, URL http://www.R-project.org. Raupach, M. J., Barco, A., Steinke, D., Beermann, J., Laakmann, S., Mohrbeck, I., … Knebelsberger, T. (2015). The Application of DNA Barcodes for the Identification of Marine Crustaceans from the North Sea and Adjacent Regions. PLoS One, 10, E0139421. Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., … Huelsenbeck, J. P. (2011). MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 1–4. Rosenblum, E. B., & Harmon, L. J. (2011). Same same but different”: Replicated ecological speciation at White Sands. Evolution, 65, 946–960. Rundell, R. J., & Price, T. D. (2009). Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends in Ecology and Evolution, 24, 394–399. Rundle, H. D., & Nosil, P. (2005). Ecological speciation. Ecology Letters, 8, 336–352. Russ, J., Loyd, D. H., & Boutton, T. W. (2000). A paleoclimate reconstruction for southwestern Texas using oxalate residue from lichen as a paleoclimate proxy. Quaternary International, 67, 29–36. Stevenson, M. M., & Peden, A. E. (1973). Description and ecology of Hyalella texana n. sp. (Crustacea: Amphipoda) from the Edwards Plateau of Texas. American Midland Naturalist, 89, 426–436. Strong, R. A. (1972). Life history variation among populations of an amphipod (Hyalella azteca). Ecology, 53, 1103–1111. Thomas, J. A., Welch, J. J., Lanfear, R., & Bromham, L. (2010). A generation time effect on the rate of molecular evolution in invertebrates. Molecular Biology and Evolution, 27, 1173–1180. Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th edn). New York, New York: Springer. ISBN 0-387-95457-0. Vergilino, R., Dionne, K., Nozais, C., Dufresne, F., & Belzile, C. (2012). Genome size differences in Hyalella cryptic species. Genome, 55, 134–139. Wellborn, G. A., & Broughton, R. E. (2008). Diversification on an ecologically constrained adaptive landscape. Molecular Ecology, 17, 2927–2936. Welton, J. S. (1979). Life-history and production of the amphipod Gammarus pulex in a Dorset chalk stream. Freshwater Biology, 9, 263–275. Westram, A. M., Panova, M., Galindo, J., & Butlin, R. K. (2016). Targeted re-sequencing reveals geographic patterns of differentiation for loci implicated in parallel evolution. Molecular Ecology, 25, 3169–3186. Witt, J. D., Blinn, D. W., & Hebert, P. D. (2003). The recent evolutionary origin of the phenotypically novel amphipod Hyalella montezuma offers an ecological explanation for morphological stasis in a closely allied species complex. Molecular Ecology, 12, 405–413. Witt, J. D., & Hebert, P. D. (2000). Cryptic species diversity and evolution in the amphipod genus Hyalella within central glaciated North America: A molecular phylogenetic approach. Canadian Journal of Fisheries and Aquatic Sciences, 57, 687–698. Witt, J. D., Threloff, D. L., & Hebert, P. D. (2006). DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: Implications for desert spring conservation. Molecular Ecology, 15, 3073–3082. Woolfit, M., & Bromham, L. (2005). Population size and molecular evolution on islands. Proceedings of the Royal Society B: Biological Sciences, 272, 2277–2282. Yang, L., Hou, Z., & Li, S. (2013). Marine incursion into East Asia: A forgotten driving force of biodiversity. Proceedings of the Royal Society B: Biological Sciences, 280, 20122892.