A phylogenetic test of sympatric speciation in the Hydrobatinae (Aves: Procellariiformes)
Graphical abstract
Introduction
Understanding the phylogenetic relationships among species can give insight into how lineages diverged and how new species arise. The process of speciation can be organized based on the geographic overlap of incipient species during divergence. These models of speciation range from complete geographic isolation of incipient species (allopatric speciation) to complete geographic overlap of incipient species (sympatric speciation) with various degrees of geographic overlap in between (peripatric and parapatric speciation; Coyne and Orr, 2004, Fitzpatrick et al., 2009). Although the importance of sympatric speciation as a mode of species generation has been controversial, recent evidence suggests that it may be more common than previously thought. For example, sympatric speciation appears to have been involved in the origin of cichlid species (e.g. Pundamilia nyererei and P. pundamilia; Seehausen and van Alphen, 1999), palm trees (Howea belmoreana and H. forsteriana; Gavrilets and Vose, 2007), subterranean blind mole rats (Spalax galili; Hadid et al., 2013), and apple maggots (Rhagoletis pomonella; Smith, 1988). Sympatric speciation by ecological segregation has also arguably occurred in birds, including Nesospiza buntings in the Tristan de Cunha archipelago (Ryan et al., 2007) and Galápagos warbler finches Certhidea olivacea and C. fusca (Tonnis et al., 2005). Sympatric speciation can also occur by allochrony, where individuals that breed at different times are less likely to encounter each other leading to reduced gene flow (Hendry and Day, 2005). For example, in sympatric periodic cicadas (Magicicada species), one population emerges on a 13-year cycle whereas another population emerges on a 17-year cycle, resulting in assortative mating and population divergence (Sota et al., 2013). Allochronic speciation can also occur as a result of populations breeding in different seasons, as in summer and winter populations of the pine processionary moth (Thaumetopoea pityocampa; Santos et al., 2011).
The Hydrobatinae (Aves: Procellariiformes; Genus: Hydrobates, Carboneras and Bonan, 2014; formerly genera Oceanodroma, Halocyptena) is a diverse subfamily of mostly Northern Hemisphere seabirds that includes several examples of genetic divergence of sympatric allochronic populations (Table 1). Both the band-rumped storm-petrel Hydrobates castro spp. (Monteiro and Furness, 1998, Snow and Snow, 1966) and Leach’s storm-petrel (H. leucorhoa; Power and Ainley, 1986) have populations that nest in different seasons (hot and cool) on the same island, often using the same burrows. Results from past and ongoing population genetic studies suggest that these seasonal populations originated sympatrically by allochrony (Friesen et al., 2007a, M.F. Silva et al., 2016; Taylor et al., unpubl.). Among other results, this led to distinction of the hot-season breeders from the Azores archipelago as a cryptic species, Monteiro’s storm-petrel (H. monteiroi; Bolton et al., 2008, Smith et al., 2007). Similarly, previous and on-going studies have found genetic differences between sympatric hot-season and cool-season populations of H. castro in the Galápagos (Smith and Friesen, 2007), H. jabejabe in Cape Verde (Deane, 2011, Friesen et al., 2007a), and H. leucorhoa in Guadalupe (H. l. cheimomnestes and H. l. socorroensis; Friesen et al., unpubl.).
The Hydrobatinae also include other potential cases of sympatric speciation among the 14 extant and one recently extinct species. Storm-petrels are pelagic, but mostly breed on isolated islands and exhibit high natal philopatry (Brooke, 2004, Warham, 1990). Breeding at their natal site can limit gene flow, likely promoting genetic differentiation between populations (Power and Ainley, 1986). Most species breed in the Northern Atlantic and Pacific oceans, while a few breed in the Southeastern Pacific (Fig. 1). H. leucorhoa and H. castro are widely distributed in both the Atlantic and Pacific (temperate, and tropical/subtropical, respectively; Brooke, 2004, Warham, 1990) with several defined subspecies and geographic variants (Table 1). Within the H. castro complex, in addition to recent recognition of H. monteiroi as a good species, H. jabejabe (previously classified under H. castro) breeding on Cape Verde has been identified as a full species (Sangster et al., 2012; Taylor et al., unpubl.). Within H. leucorhoa, four subspecies have been recognized: H. l. socorroensis, hot season breeder on Guadalupe I.; H. l. cheimomnestes, cool season breeder on Guadalupe I.; H. l. chapmani, hot season breeder on islands off Baja California; and H. l. leucorhoa, which breeds throughout the North Atlantic and North Pacific oceans (Power and Ainley, 1986). In the North Pacific, the fork-tailed storm-petrel (H. furcata) breeds around the Aleutian Islands and the Pacific coast of Canada (Brooke, 2004, Warham, 1990). In the North Atlantic, one subspecies of European storm-petrel (H. pelagicus pelagicus) breeds in the Atlantic and the other subspecies (H. p. melitensis) breeds in the Mediterranean (Cagnon et al., 2004, Sangster et al., 2012).
Storm-petrels appear to have a few major hotspots of diversity (Fig. 1). For instance, many storm-petrel species breed in the waters around Baja California, Mexico including the least storm-petrel (H. microsoma), black storm-petrel (H. melania), ashy storm-petrel (H. homochroa), three subspecies of H. leucorhoa, and the recently extinct H. macrodactyla (Brooke, 2004, Warham, 1990). A diversity hotspot also occurs off the coast of Peru, where Markham’s storm-petrel (H. markhami), and one wedge-rumped storm-petrel subspecies (H. tethys kelsalli) breed (Brooke, 2004, Warham, 1990). The other wedge-rumped storm-petrel subspecies (H. tethys tethys) breeds around the Galápagos (Brooke, 2004, Warham, 1990). The breeding range of Hornby’s storm-petrel (H. hornbyi) is unknown as nests have not been found; however observations of it in the waters around Chile and Peru, and observations of fledglings inland, suggest that it nests in this area (Brooke, 1999).
Another hotspot of diversity occurs in the Northwestern Pacific around Japan where Matsudaira’s storm-petrel (H. matsudairae), Swinhoe’s storm-petrel (H. monorhis), Tristram’s storm-petrel (H. tristrami), H. leucorhoa, and H. castro breed (Brooke, 2004, Warham, 1990). Similar to H. castro on the Azores archipelago, these species breed in different seasons in the same geographic area (Brooke, 2004). H. tristrami breeds in the cool season from October to June on northwestern Hawaiian Is. and on islands in the Ogasawara Archipelago of Japan (McClelland et al., 2008). H. matsudairae also breeds in the cool season but has a breeding range restricted to Iwo Island (Chiba et al., 2007). Historically, H. matsudairae and H. tristrami bred sympatrically on Iwo I., but their current breeding sites do not overlap (Chiba et al., 2007, Ornithological Society of Japan, 2012). H. monorhis breeds in the hot season from June to October (Brooke, 2004) on islands off of Japan, Korea, far east Russia, and China, with its largest breeding colony on Kutsujima I. in the Sea of Japan (Ornithological Society of Japan, 2012, Sato et al., 2010). Currently, H. tristrami and H. monorhis breed sympatrically at two breeding sites (Hachijo-Kojima I. and Kozushima I.) but in different seasons (McClelland et al., 2008, Ornithological Society of Japan, 2012, Sato et al., 2010). The difference in breeding times between these species in the same geographic area suggests they may have arisen through sympatric speciation by allochrony.
Despite these interesting geographic distributions, the phylogenetic relationships among the species are not well characterized, with only a few partial phylogenies (e.g. Friesen et al., 2007a, Friesen et al., 2007b, M.C. Silva et al., 2016, Nunn and Stanley, 1998, Penhallurick and Wink, 2004). For the present study, we used gene trees and a multispecies coalescent model (∗Beast; Degnan and Rosenberg, 2009, Heled and Drummond, 2010) based on one mitochondrial segment and five nuclear introns to estimate phylogenetic relationships among all extant species and subspecies (Table 1). Specifically, given previous evidence for sympatric speciation by allochrony (above), we used a phylogenetic approach to test whether the sympatric species with non-overlapping breeding seasons in Japan (H. tristrami in the cool season and H. monorhis in the hot season) may have arisen through sympatric speciation by allochrony. In addition, we tested whether species breeding in the same geographical area (e.g. Peru, Baja California area) are monophyletic as predicted under sympatric speciation.
Section snippets
Sample collection and DNA extraction
Tissue, feather or blood samples were obtained for representatives of all extant species of the storm-petrel subfamily Hydrobatinae (Table 1). At least two individuals per species were included in our analysis. Whenever possible, two individuals from each named subspecies or previously identified genetically differentiated conspecific population were also included (e.g. Cagnon et al., 2004, Smith et al., 2007). We also attempted to extract DNA from museum specimens of H. macrodactyla; however,
Sequence variation
Sequences of the entire MT-CYB gene, 1143 bp including 396 variable sites, were obtained from 46 individuals (GENBANK: KU217327–KU217371). Sequence ambiguity was found at only one site and may be due to true mitochondrial (mtDNA) heteroplasmy or a sequence artifact, and was coded as missing data. Several lines of evidence indicated that mtDNA was amplified, as opposed to nuclear homologs of mtDNA (numts; following Friesen and Anderson, 1997), including that sequences of some species were either
Discussion
According to Coyne and Orr (2004), four criteria must be met for sympatric speciation to be inferred: the species must (1) have sympatric distributions, (2) be mostly reproductively isolated, (3) exhibit a sister relationship, and (4) have had little chance of an allopatric phase in their history. In the present study, the MT-CYB tree provided high support for the previously found sister relationship between cool-season (H. castro) and hot-season (H. monteiroi) band-rumped storm-petrels from
Acknowledgements
The authors would like to thank M. Atkey, T. Boulinier, P. Deane, B. Furness, J.A. Gil-Delgado, E. Gómez-Díaz, O. Hasegawa, Y. Kolbeinsson, K. McCoy, L. Monteiro, V. Neves, N.N. Pavlov, R.L. Pitman, A. Quesada, A. Smith, and S.V. Zagrebelny for sample collection. Permissions for sample collection were given by State National Biosphere Reservate Nicolskoe (Kamchatka, Russia), Govern Balear (Spain), and Spanish Polar Committee. Thank you to M. Peck at the Royal Ontario Museum, J. Trimble at
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Cryptic species and independent origins of allochronic populations within a seabird species complex (Hydrobates spp.)
2019, Molecular Phylogenetics and EvolutionCitation Excerpt :Fiser et al. (2018) suggest three predictions if PNC is the cause of morphological stasis: morphological constraint due to selection; similar ecological niches among the cryptic taxa; and speciation in allopatry. The band-rumped storm-petrel species complex (genus Hydrobates, previously Oceanodroma - all species within the Hydrobatinae were recently subsumed within the genus Hydrobates by the European Taxonomic Commission - see Wallace et al., 2017 for a phylogeny) presents an excellent opportunity to investigate drivers of cryptic divergence. Band-rumped storm-petrels are small, highly pelagic seabirds with a widespread distribution, breeding on tropical and sub-tropical islands in the Atlantic and Pacific Oceans (Brooke, 2004; Smith et al., 2007; Fig. 1).
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Current address: School of Health Sciences, St. Lawrence College, Brockville, Ontario K6V5X3, Canada.