INTRODUCTION
Speciation is a key evolutionary process that results from the
independent evolution and adaptation of populations and ultimately acts
as a major driver responsible for the generation of species-level
biodiversity (Kopp,
2010; Schluter & Pennell, 2017). Species richness is unevenly
distributed across the Tree of Life, and its current patterns of
distribution result from biotic and abiotic processes that operate over
space and time
(Benton, 2009;
Simpson, 1953; Vargas & Zardoya, 2014). Evidence for the mechanisms
that promote population differentiation and speciation are currently
better understood in terrestrial than in marine environments
(Butlin et al.,
2012; Coyne & Orr, 2004; Nosil, 2012), where the lack of obvious
physical barriers would suggest that neutral processes of panmixia, or
isolation-by-distance, will prevail, especially in highly mobile species
(Moura et al., 2013).
However, counterintuitive evidence of fine-scale differentiation among
populations and species in a number of marine taxa has been described as
the “marine species paradox”
(Bierne, Bonhomme, &
David, 2003; Palumbi, 1994). Thus, there is a need for explicit
evaluations of the role of selective processes in driving patterns of
differentiation in marine systems.
In species complexes that are geographically widespread, the gradual
evolution of reproductive isolation in allopatry can make species
delimitation challenging, especially in young radiations
(Carstens, Pelletier,
Reid, & Satler, 2013; Cutter, 2013). Many allospecies first tend to
differ from their close relatives at traits subjected to sexual and
other forms of social selection
(Price, 2008; Seddon et
al., 2013). When this occurs, our ability to delimit species may be
further hampered by morphological stasis, especially when changes in
ecological niche in allopatry are minimal
(Fišer, Robinson, & Malard,
2018). In cases of morphological stasis and limited behavioural
information, genomic data can provide informed hypotheses on species
limits of allopatric taxa and can be conclusive in parapatric or
sympatric taxa. Despite the extent of disagreement about how genomic
data should be applied to species delimitation
(Leaché, Zhu, Rannala,
& Yang, 2018; Sukumaran & Knowles, 2017), agreement exists that
genomic data can provide additional perspective on species limits when
used together with other data types such as phenotypic and ecological
information.
Seabirds of the order Procellariiformes present some of the most extreme
examples of the marine speciation paradox. Procellariiformes are highly
mobile pelagic seabirds with a high dispersal ability and perform some
of the longest animal migrations on Earth (covering more than 120,000 km
a year) (Shaffer et al.,
2006; González-Solís, Croxall, Oro, & Ruiz, 2007; Weimerskirch, Delord,
Guitteaud, Phillips, & Pinet, 2015). However, Procellariiformes also
show high philopatry to their breeding grounds
(Coulson, 2002), which is
expected to limit gene flow and therefore reinforce genetic
differentiation (Friesen,
Burg, & McCoy, 2007).
Shearwaters are a monophyletic group in the family Procellariidae, and
they offer an excellent case study for examining the mechanisms of
population differentiation and speciation in marine environments. First,
shearwaters are globally distributed and breed mostly in allopatry.
Second, the current taxonomy recognises three genera and 30 species with
a well-resolved phylogeny showing clear periods of rapid diversification
(Ferrer-Obiol et al. under review). Third, the three recognised genera
exhibit different ecologies and degrees of species richness. Fourth,
their high mobility makes them an ideal model to evaluate the roles of
founder events and vicariance using biogeographic analyses. Fifth,
abiotic and biotic factors are known to promote speciation in the
shearwaters and related Procellariiformes; for instance,
paleoceanographic changes such as the Pleistocene climatic oscillations
can act as historical drivers of speciation
(Gómez-Díaz,
González-Solís, Peinado, & Page, 2006; Silva et al., 2015) and
intrinsic biotic factors such as different foraging strategies and
allochrony can also promote speciation
(Friesen, Smith, et
al., 2007; Lombal, Wenner, Lavers, & Austin, 2018; Rayner et al.,
2011). Sixth, species limits are controversial, mostly due to high
morphological stasis
(Austin, Bretagnolle, &
Pasquet, 2004; Austin, 1996); indeed, only a few phenotypic traits,
such as vocalisation characteristics, slight plumage colour differences
and in particular, body size, may differ between closely related
species. A comprehensive study using genomic data will assist in
resolving species delimitation within the context of the factors that
promote diversification and speciation.
To accurately relate historical environmental and oceanographic changes
to the timing of speciation events, it is necessary to estimate accurate
divergence times. Analyses based on concatenation can lead to biases in
branch lengths and misleading age estimates, particularly at recent
timescales (Angelis
& Dos Reis, 2015; McCormack, Heled, Delaney, Peterson, & Knowles,
2011; Mendes & Hahn, 2016). For such events, the multispecies
coalescent model (MSC) offers a more accurate solution by incorporating
the effects of incomplete lineage sorting (ILS), which is likely the
most common source of phylogenetic incongruence in rapid diversification
events (Edwards et
al., 2016; Maddison, 1997; Suh, Smeds, & Ellegren, 2015).
The reconstruction of ancestral ranges and evaluation of alternative
biogeographic models are critical to our understanding of shearwater
diversification throughout the world in light of environmental and
oceanographic events. Of particular interest is the importance of
founder events during the evolution of shearwaters. The foundation of
colonies is believed to be a rare event in most seabird species despite
their great potential for long-range dispersal (Milot, Weimerskirch, &
Bernatchez, 2008). However, in several shearwater species, contemporary
colony foundation events have been reported (Munilla, Genovart, Paiva,
& Velando, 2016; Storey & Lien, 1985). Understanding the relative
importance of founder and vicariant events during the evolution of
shearwaters can have important implications for the conservation of
these endangered pelagic seabirds.
Here, we use paired-end double-digest restriction site-associated DNA
sequencing (PE-ddRAD-Seq) for almost all extant shearwater taxa to
explore the drivers of diversification and speciation in this group of
pelagic seabirds. Specifically, we produce the first time-calibrated
shearwater species tree using the MSC to account for the high levels of
ILS affecting the shearwater phylogeny. We then infer the biogeographic
history of the group by estimating ancestral ranges and evaluating the
roles of founder events, vicariance and surface ocean currents in
driving their diversification. Furthermore, we explore the ecological
forces responsible for the variability in a key phenotypic trait, body
size. Finally, we assess the validity of the current taxonomy of the
group by analysing genomic patterns of recent shared ancestry and
differentiation among shearwater taxa.