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Journal of Biogeography. 2022;00:1–14. wileyonlinelibrary.com/journal/jbi
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1© 2022 John Wiley & Sons Ltd.
Received: 23 September 2021
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Revised: 10 June 2022
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Accepted: 14 June 2022
DOI : 10.1111/j bi.14 464
SYNTHESIS
Genetic impacts of physical disturbance processes in coastal
marine ecosystems
Elahe Parvizi1 | Ceridwen I. Fraser2 | Jonathan M. Waters1
Handling editor: Greer D olby
1Department of Zoology, University of
Otago, D unedin, New Zealand
2Depar tment of Marine S cience,
University of Otago, Dunedin, New
Zealand
Correspondence
Elahe Parvizi, Department of Zoology,
University of Otago, PO Box 56, Dunedin
9054, New Zealand.
Email: ellie.par vizi@gmail.com
Funding information
Ruther ford Fellowship; University of
Otago; Roy al Society of New Zealand;
Marsden Fund
Abstract
Aim: Coastal habitats are among the most dynamic environments on earth and are
highly vulnerable to large-scale physical disturbance. Genetic studies of nearshore
marine species are revealing long-lasting signatures of major coastal disturbance
events. We synthesize emerging data to highlight how physical perturbations can im-
pact the phylogeographic patterns of coastal populations.
Tax o n: Coastal marine and estuarine taxa.
Location: Coastal regions around the globe.
Methods: We synthesize coastal genetic and genomic literature, focussing particu-
larly on the phylogeographic consequences of natural disturbance events including
uplift, tsunami, hurricanes, glaciations and sea-level fluctuations. We focus on studies
with clear physical analytical frameworks constrained by abiotic data.
Results: Tectonic and atmospheric disruptions can be considered shot-term events
with major impacts on populations adjacent to the centre of disturbance, typically
resulting in the evolution of shallow phylogeographic patterns. Long-lived climate-
driven disturbances such as glaciations, however, operate over vast geographic scales
and often drive deep evolutionary patterns in affected populations. We show that
studies using genome-wide data could better identify fine-scale signatures of both
past and contemporary habitat perturbations.
Conclusions: Recent data reveal the interplay between physical upheaval and coastal
phylogeography, indicating that disturbance can affect diversity, connectivity and de-
mography of coastal populations. The interplay between long-lived large-scale dis-
turbance and species-specific biotic traits has shaped deep phylogeographic patterns
of coastal taxa. Additionally, it could be argued that, at least for some regions, short-
term disturbance is the ‘rule’ rather than the ‘exception’, and thus, represents a key
driver of coastal genetic patterns in disturbance prone coastal regions. Geo-genomic
approaches that combine genome-wide data with explicit habitat models or distur-
bance history information have been particularly successful in explaining the driv-
ers of coastal evolutionary change. We argue that future integration of genomic and
physical data will be crucial for tracing evolutionary trends in fast-changing marine
environments.
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Parvi zi et al.
1 | THE LAND- SEA INTERFACE IS
PARTICULARLY VULNERABLE TO
DISTURBANCE
Earth's coastlines are transition zones between land and ocean, and
they are the domain of constant habitat change driven by differ-
ent terrestrial, oceanic and atmospheric processes. Contemporary
coasts are geologically young, having mainly developed during the
Holocene following the broad stabilization of eustatic sea- levels
approximately 7000– 5000 y BP (Clark et al., 1978; Peltier, 2002).
Coastal zones encompass all near- shore marine, shoreline, and mar-
itime terrestrial habitats (Doody, 2001), comprising different types
of ecosystems such as estuaries, mangroves, seagrass, near- shore
reefs, intertidal and subtidal benthic habitats, algal beds and near-
shore pelagic waters (Sheaves, 2009). Coastal ecosystems are often
highly productive and provide a range of ecosystem services related
to fisheries, tourism, recreation, education and research, bringing
important economic and biodiversity benefits (Barbier et al., 2011).
These heterogeneous, marginal habitats have proven particularly
interesting for bio- and phylogeographers for several reasons. For
instance, these habitats are geographically constrained and spatially
fragmented and yet, subject to dynamic physical disturbance pro-
cesses operating over a broad variety of spatial scales.
The boundaries of coastal ecosystem units are controlled by tec-
tonic, sedimentary, and sea- level processes, and forces arising from
changing waves and current regimes (Dolby et al., 2020; Ray, 2005).
Tectonic and sea- level processes can modify the geomorphic prop-
erties of continental shelves, and those properties, in turn, restrict
ecosystem boundary conditions and control where different types
of coastal habitats can form (Algeo & Wilkinson, 1991; Dolby
et al., 2020; Parvizi et al., 2019; Ray, 2005). External oceanic and
atmospheric forces including storms and hurricanes, on the other
hand, can profoundly affect the distribution range and dispersal pat-
terns of taxa, change the structure and diversity of communities, and
potentially contribute to the emergence of novel coastal ecosystems
and dispersal of exotic species to coastal areas around the globe
(Doney et al., 2012; Fraser, Morrison, et al., 2018; Smith et al., 1999).
Some coastal regions (e.g. equatorial waters) can be specifically
characterized by ongoing atmospheric disturbances, with cyclonic
storms being typical, synoptic weather patterns under which the
physical structure and biotic features of coastal ecosystems are con-
stantly affected (Michener et al., 1997 ).
Many coastal habitats (e.g. estuarine, intertidal) are particu-
larly vulnerable to disturbance processes. Although the biological
assemblages of such zones have adapted to withstand frequent
shifts in sea- levels, temperatures, salinity and desiccation stress
(Ray, 2005; Thomsen et al., 2019; Thorner et al., 2014), coastal taxa
are often ecologically specialized, frequently restricted to localized
habitats— for example, narrow intertidal bands— and are thus poten-
tially highly vulnerable to the effects of environmental disturbance.
These spatial constraints provide strong model systems for assessing
biodiversity shifts linked to past and contemporary habitat changes
(Clausing et al., 2000; Kadereit & Westberg, 2007).
In coastal ecosystems, recognizing the environmental mech-
anisms underpinning biodiversification is challenging mainly due
to the complexity of physical processes at the land- sea interface.
Indeed, intense anthropogenic impacts on coastal regions can
sometimes obscure any underlying natural ecosystem shifts (He &
Silliman, 2019). Additionally, the high levels of biological and physi-
cal variability that happen across various temporal and spatial scales
can obscure distinguishing the “normal” state or range of coastal
systems (Talley et al., 2003). As a result, the integration of genetic /
genomic data with novel methods of studying landscape change can
provide powerful tools to enhance our understanding of physical
and biological dynamics in coastal ecosystems.
In this review, we have two major goals. First, to synthesize ev-
idence emerging from recent phylogeographic analyses of coastal
taxa to understand how major disturbances— including tectonic,
atmospheric and climatic events— can affect marine populations
inhabiting coastlines along continental margins. Here, we adopt
White's (1979) definition of ‘disturbance’ as catastrophic and irreg-
ular events originating in the physical environment. We also define
disturbance phylogeography as the study of physical disruption im-
pacts on the distribution of genetic lineages. This synthesis will focus
primarily on natural exogenous factors that disturb coastal habitats,
and thus does not include anthropogenic or biotic (e.g. disease out-
break) disruptions. Second, we aim to assess the potential of geo-
genomics approaches (Dolby et al., 2022) that integrate genomic and
geological or climatic data for reconstructing disturbance histories.
We highlight how geo- genomics can provide a strong framework
for identifying regional physical anomalies that control evolutionary
patterns in coastal populations.
2 | COASTAL GENETIC SIGNATURES OF
CATASTROP H I C TECTONI C P ROCESSES
Near- shore fault rupture events can cause vertical movement of
the continental margin (uplift or subsidence), change the position
of coastlines or invoke landslides and subsequent debris runouts
(Clark et al., 2017; Plafker & Savage, 1970). In particular, coastal up-
lift can displace near- shore ecosystem boundaries by shifting the
vertical zonation of tidal ranges, leading to the exposure of biota to
acute physical stress such as increased temperature, desiccation or
turbidity (Schiel et al., 20 19). These can have catastrophic ecosys-
tem consequences including the loss of key species, disruptions to
KEY WORDS
earthquake, environmental disturbance, geobiology, heat- wave, marine biogeography,
Pleistocene
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Parvizi et al .
community connectivity and reduced ecosystem functioning (Schiel
et al., 2019). Earthquakes can displace non- dispersive benthic com-
munities and, depending on the magnitude of land- level change
and shore type, lead to regional extirpation of intertidal and shal-
low subtidal biota (Chunga- Llauce & Pacheco, 2021; Figure 1a). On
rocky shores, for instance, observations from the 2016 Kaikōura
earthquake in southern New Zealand showed extensive coastal
uplift can cause local extirpation of rocky reef communities (Peters
et al., 2020; Schiel et al., 2019), providing new empty intertidal habi-
tats for the recolonization of dispersing genetic lineages in the dis-
turbed zone (Peters et al., 2020). The co- seismic subsidence of rocky
intertidal zone following the 2011 Great East Japan earthquake
immediately shifted some sessile coastal invertebrates downward
and decreased the abundance of several sessile and mobile species
(Noda et al., 2016). Chile's 2010 earthquake reportedly drowned
sandy beaches on coasts along the northern rupture segment due to
subsidence and subsequent tsunami, while expanding and flattening
beaches along the co- seismically uplifted southern rupture, both of
which significantly deteriorated sandy beach ecosystems (Jaramillo
et al., 2012). The effects of Chile's 2010 earthquake on rocky shore
ecosystems have been documented by comparing pre- and post-
quake microsatellite data of the red alga Agarophyton chilense, which
showed an immediate loss of rare alleles following the uplift and ge-
netic recovery after 2 years in non- cultivated populations (Becheler
et al., 2020). Similarly, fine- scale SNP sampling of three southern bull
kelp species (Durvillaea spp.) along prehistorically disturbed rocky
shores in southern New Zealand has detected uplifted- associated
genetic impacts in intertidal (but not subtidal) species (Figure 1a;
Parvizi et al., 2020). Additionally, comparative phylogeographic
analysis of these kelps together with their epibiota has revealed sig-
natures of concerted recolonization events following this ancient
ecosystem- wide disturbance (Parvizi et al., 2022).
In addition to the displacement of tidal ranges on uplifted coastal
blocks, coastal tectonic disturbances can cause landslide and conse-
quent rockfall deposits, potentially providing new coastal habitats
for recolonization of non- native lineages or taxa. Extensive field
sampling and fine- scale genome- wide SNP analysis of the intertidal
macroalga, Durvillaea poha in New Zealand have reported a small
population outside the common geographic range of this species
(Vaux et al., 2021). This small population occurs along geologically
disturbed coastlines of the North Island, suggesting that earthquake-
generated landslides created an opportunity for a northward range
expansion event in D. poha (Vaux et al., 2021). Furthermore, sud-
den large- scale earthquakes can isolate near- shore populations on
uplifted habitats and provide opportunity for genetic diversification
along seismically disturbed sites (Lescak et al., 2015). For example,
the 1964 earthquake in Alaska uplifted submarine terraces along
multiple islands and isolated new freshwater habitats. SNP com-
parison between threespine stickleback fish, Gasterosteus aculeatus
on the uplifted habitats and their coastal ancestors showed strong
genomic divergence and revealed one of the most rapid specia-
tion events recorded in response to sudden seismic disturbance in
coastal ecosystems (Lescak et al., 2015).
Coastal evolutionary impacts of volcanic eruptions have been re-
ported for two coral reef- dwelling mantis shrimp taxa (Haptosquilla
pulchella; H. glyptocer) in the island of Krakatoa, west of Java (Barber
FIGURE 1 Examples of coastal evolutionary responses to tectonic and oceanographic disturbance processes. (a) Co- seismic coastal
uplift can modify the vertical zonation of intertidal habitats, resulting in local extirpation of uplifted populations. New intertidal habitats
can be recolonized by lineages that are genetically distinct from pre- uplift populations. (b) Tsunami and cyclones can enhance population
connectivity and reduce isolation by distance. (c) Tsunami and cyclones can facilitate dispersal over long distances and drive potential
geographic range shifts.
Evolution of
(b)
Transporting
Potential
(c)(a)
new spatial
sector
Range limit
geographic
expansion
Range limit
Coastal uplift
extirpates
Faultline Faultline
Transporting
Reduced
Increased
populations
Faultline Faultline
larvae
or adults
isolation by
distance
genetic
admixture
larvae
or adults
genomic
uplift
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Parvi zi et al.
et al., 2002). MtDNA comparisons between areas affected versus
unaffected by the 1883 Krakatoa eruption reveal strong signatures
of recolonization and demographic expansion in the former pop-
ulations, indicating larval dispersal can contribute to rapid post-
disturbance recovery (Barber et al., 2002).
3 | INDIRECT EFFECTS OF TECTONIC
PROCESSES: POST- EARTHQUAKE TSUNAMI
Tsunami events can cause sudden flooding and dramatically change
coastal habitats. The vulnerability of near- shore ecosystems to tsu-
nami depends on coastal topographic characteristics such as ba-
thymetry and orientation, wave directionality and relative distance
to tsunami epicentre (Reynolds et al., 2017). Large tsunami waves
can cause sediment erosion, change sediment composition and sub-
sequently result in major habitat loss in coastal areas (Chunga- Llauce
& Pacheco, 2021). Such a habitat loss is likely to be short- lived, but
it can provide opportunities for founder events and subsequent
turnover in local community assemblages. A long- term microsatel-
lite genetic survey of the mud snail, Batillaria attramentaria in Japan
showed that the 2011 Tohoku tsunami caused declines in the effec-
tive populatio n size of dist urbed populations, but it did not alter geo-
graphic genetic structure after the tsunami, suggesting there were a
large number of survivors, possibly because of the complex topog-
raphy of the bays which created micro- refugia (Miura et al., 2017).
The evolutionary consequences of tsunamis on coastal biota are also
determined by species traits such as habitat choice and dispersal/
survival potential of adults or larvae, as was observed in idiosyn-
cratic genetic responses of Chilean sandy beach crustaceans to the
2010 tsunami (Brante et al., 2019). Finally, tsunamis can alter coastal
spatial distribution patterns and enhance population connectivity,
especially in species with long- lasting propagules (Figure 1b). For ex-
ample, the 2011 Tohoku tsunami created new tidal marsh habitats,
promoted gene flow between geographically neighbouring popula-
tions and, by releasing soil seed banks, improved microsatellite allelic
richness in newly emergent post- tsunami populations of the tidal
marsh plant, Carex rugulosa (Ohbayashi et al., 2017).
4 | GENETIC EFFECTS OF OCEANIC AND
ATMOSPHERIC PROCESSES
Hurricane and cyclonic disturbances can cause storm surge and
depending on speed, intensity, direction of approach and point of
landfall, they can have major effects on coastal areas (Greening
et al., 2006; Weisberg & Zheng, 2006). Rather than being seen as
‘anomalous’ processes, hurricane and cyclones should arguably be
considered central features of many tropical coasts, with ongoing
impacts on coastal ecosystem structure and dynamics (Michener
et al., 1997). The destructive ecosystem consequences of such dis-
turbances include changing the environmental factors of coastal
habitats (e.g. water quality and salinity), physical damage (e.g.
shoreline and dune erosion), habitat fragmentation, and increasing
species mortality and dispersal (Greening et al., 2006).
Genetic analyses of the effects of hurricane- induced distur-
bances have sometimes found evidence for increased genetic ad-
mixture among affected populations (Figure 1b). For example,
the comparison of pre- and post- hurricane genetic data from sail-
fin molly, Poecilia latipinna in north Florida showed that the 2005
Hurricane Dennis erased patterns of isolation by distance that were
present in 1985, apparently via long- shore transportation of individ-
uals (Apodaca et al., 2013). Specifically, the hurricane caused an ab-
normally large storm surge and, rather than pushing water towards
the shore, moved it laterally along the coastline which resulted in
long- distance (up to 40 km) redistribution of coastal populations
(Apodaca et al., 2013). Another pre- and post- hurricane mtDNA
sequence comparison has also revealed enhanced gene- flow and
higher post- disturbance genetic diversity in the dispersal- limited
isopod, Gnathia marleyi following the 2017 hurricanes in the north-
eastern Caribbean (Pagán et al., 2020).
Hurricanes and severe storm events can potentially drive range-
shifts and geographic expansion in species with long- distance dis-
persal ability (Figure 1c). MtDNA sequencing of beach- cast kelps
following the 2017 southerly storm in New Zealand showed that
the storm disrupted the oceanographic barrier between cold, sub-
Antarctic and warm, temperate waters (i.e., the subtropical front)
by transporting substantial numbers of sub- Antarctic Durvillaea
rafts and their epibiotic passengers to the southeast coasts of New
Zealand (Waters et al., 2018). Likewise, SNP analyses of beach-
cast bull kelp reaching Antarctica, combined with oceanographic
models incorporating wind- forced wave transport, revealed that
storms were almost certainly responsible for the rafts' ability to
cross oceanographic frontal ‘barriers’ (Fraser, Morrison, et al., 2018).
Furthermore, the 2017 Hurricane Irma reportedly dispersed black
mangrove propagules well beyond this species' normal range mar-
gin (Kennedy et al., 2020). An extensive microsatellite genotyping
of the beach- stranded propagules showed they had drifted from the
nearest source populations and suggested that large hurricanes can,
in long- term, facilit ate poleward range shift of mangroves and deter-
mine their expanding gene pool (Kennedy et al., 2020).
Thermal stress associated with heatwaves is increasingly af-
fecting coastal areas. Rapid increases in seawater temperature can
exceed species' physiological thresholds and cause severe mass
mortalities, local extinctions and range contractions (Garrabou
et al., 2009; Smale & Wernberg, 2013; Thomsen et al., 2019) or even
alter the benthic ecosystem structure and biodiversity patterns
(Wernberg et al., 2013). Anomalous marine heatwaves that drive
sudden population extirpation are associated with loss of genetic
diversity in disturbed zones. For example, microsatellite data inte-
grated with environmental regression models using variables that
affect the physiology of a red gorgonian in the Mediterranean sea
showed the low genetic diversity of shallow populations most likely
arises from thermal stress caused by sudden marine heatwaves
(Pilczynska et al., 2019). Similarly, extremely high sea- surface tem-
peratures during the 1982/83 El Niño have left negative genetic
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Parvizi et al .
impacts on the intertidal kelp, Lessonia nigrescens in northern Chile
by reducing heterozygosity and polymorphism in RAPD markers to
less than half in highly disturbed sites compared to non- affected
sites (Martínez et al., 2003). More recently, heatwaves in the Pacific
had major ecological and biogeographic effects on coastal marine
biota. In the northeast Pacific, sudden sea surface temperature
anomalies have affected fish abundance and diversity and invoked
biogeographic shifts and changes in species composition (Nielsen
et al., 2021; Thompson et al., 2021). In some cases, marine heat-
waves can promote poleward range shifts. For example, the 2011
heatwave in Western Australia apparently enhanced recruitment of
the rocky reef fish Choerodon rubescens in more southern (cooler)
areas (Cure et al., 2017). Although SNP analyses suggested that re-
cruits originating from warmer parts of the range of this species had
limited survival in the south, such shifts nevertheless likely play a
key role in biogeographic responses to thermal disturbance (Cure
et al., 2017). In some cases, recurrent thermal stress can drive local
adaptation and enhance species tolerance against heat. In particu-
lar, seascape genomic studies on coral reefs have provided remark-
able insights such as identifying genomic regions (e.g. heat- shock
genes) and molecular mechanisms (e.g. DNA damage- repair) asso-
ciated with heat and bleaching tolerance and predicting individual
bleaching responses under future climate change (Fuller et al., 2020;
Selmoni et al., 2020, 2021).
5 | ANCIENT DISTURBANCES: HIGH-
LATITUDE GENETIC SIGNATURE OF
GLACIAL IMPACT
Many high- latitude coastlines were covered by expanding glaciers
during the last glacial maximum (LGM) at around 25– 18 ka (Clark
et al., 2009). With the advancement of ice sheets, high- latitude pop-
ulations contracted their ranges to temperate glacial refugia, and
subsequently moved back towards poles as ice sheets receded dur-
ing interglacials (Figure 2a; Hewit t, 2000). Such poleward range ex-
pansion and serial founder events along recolonization routes have
created strong contemporary genetic patterns with lower diversity
in younger, higher- latitude populations. Although the general rule
of glacial contraction and postglacial expansion has been reported
for some cold- temperate coastal taxa of both northern and south-
ern hemispheres, the patterns are not always simple (e.g. Allcock
& Strugnell, 2012; Fraser et al., 2012; González- Wevar et al., 2013,
2021; Maggs et al., 2008). Rising sea levels— some 120 m since the
LGM— have obscured many records of past distributions (Maggs
et al., 2008; Marko, 200 4), and the physical complexity and regional
heterogeneity of coastal systems reflect idiosyncratic glacial histo-
ries in different high- latitude coasts.
During the LGM, the Atlantic coast of North America had lim-
ited rocky habitat and relatively compressed isotherms compared to
Europe's Atlantic coast (Ingolfsson, 199 2; Olsen et al., 2010; Wares
& Cunningham, 20 01). This contrast implies that northwest Atlantic
populations of amphi- Atlantic coastal species were likely more af-
fected by glacial conditions than their counterparts in the northeast
Atlantic, resulting in the evolution of more homogeneous genetic
patterns (lower diversity) in several intertidal species of the former
region (Bowen et al., 2016; Henzler & Ingólfsson, 2008; Wares &
Cunningham, 2001). In contrast, recent ice- sheet reconstructions
suggest the presence of ice- free coastlines along the Atlantic coasts
of Canada (Charbit et al., 2007) which, presumably, allowed the exis-
tence of ice- free rocky shores during the LGM and facilitated in situ
persistence of some intertidal taxa in high- latitude refugia. Genetic
consequences of such northwest Atlantic refugia, for instance, in-
clude the deep phylogeographic break between the northwest
FIGURE 2 Examples of genetic
signatures of glacial disturbance (a) high
latitudes versus (b) temperate regions. (a)
Habitat loss due to glacier advance during
glaciations followed by range expansion
during interglacial, resulting in low genetic
diversity and demographic bottleneck
in affected populations. (b) Habitat loss
due to coastal morphodynamics during
glacial– interglacials resulted in the
isolation of populations and evolution of
genetic structures along coasts without
contemporary barriers to gene- flow.
Lower Latitudes
Higher Latitudes
Glacier retreat
and range expansion
Interglacial
Glacial
(a)
ice sheet
gene-flow
sandy beach
Uninhabitable
phylogeographic break due to
historical coastal vicariance
Interglacial
Glacial
(b)
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Parvi zi et al.
Atlantic and northeast Atlantic populations of the marine snail,
Littorina saxatilis (Panova et al., 2011) or the presence of private al-
leles and haplotypes on both sides of the Atlantic in populations of
the fucoid seaweed, Ascophyllum nodosum (Olsen et al., 2010).
Glacial geology of the northeast Pacific suggests the presence
of ice- free patches of coastline during the LGM, so intertidal habi-
tats existed along exposed lands among coastal glaciers (Luternauer
et al., 1989; Marko, 2004). Such scattered intertidal habitats may
have provided local refugia in high latitudes of the northeast Pacific
and resulted in regional genetic differentiation. Long- term demo-
graphic stability of benthic taxa in Alaska's local refugia have been
detected by studying mtDNA sequence data of the gastropod,
Nucella lamellosa (Marko, 20 04) and several rocky- shore species
(Marko et al., 2010 ). Phylogeographic studies of a number of sea-
weeds in the northeast Pacific similarly support the presence of
local refugia within the region. For instance, broad multilocus phy-
logeographic analyses (spanning 2800 km) of Alaskan (Pacific coast)
Alaria showed high diversity among populations and departure from
neutrality, suggesting the local persistence of populations during
glaciations (Grant & Bringloe, 2020). Similarly, multilocus analyses
of split kelp (Hedophyllum nigripes) and sugar kelp (Saccharina latis-
simi) support northern ice- age refugia in the Gulf of Alaska (Grant
et al., 2020; Grant & Chenoweth, 2021).
In the high- latitudes of the Southern Hemisphere, there is a
longstanding view that the majority of extant benthic communities
survived severe glacial advances in southern high- latitude refugia
(Clarke et al., 1992; Lau et al., 2020). The hypothesized coastal refugia
were likely located at ephemeral unglaciated areas of the Antarctic
continental shelf break, open- ocean polynyas, continental slope,
deep- ocean basins, and adjacent sub- Antarctic Islands or southern
South America (Allcock & Strugnell, 2012; Brey et al., 19 96; Clarke
et al., 1992; Fraser et al., 2012; Lau et al., 2020; Thatje et al., 2005,
2008). Phylogeographic studies along high- latitude coastlines of the
Southern Ocean have reported a clear link between contemporary
genetic divergence and historical distribution of the coastal LGM
ice sheets. Those studies show correspondence with geological un-
derstanding of the extent of the Patagonian and sub- Antarctic ice
sheets at the LGM, and they also shed light on the extent of sea
ice, which was less well known based solely on geological data
(Figure 2a; Fraser et al., 2010, 2012; Macaya & Zuccarello, 2010 ).
6 | ANCIENT DISTURBANCES: GENETIC
SIGNATURES OF SHIFTING SEA- LEVELS
Although temperate and tropical coasts remained largely unglaciated
throughout the Pleistocene, coastal habitat type and configuration
in these areas have been greatly transformed as a result of glacial
expansion/contraction cycles. Some temperate coasts experienced
major transitions between cold, rocky or cobbled shores during
glacial periods and warm, sandy shores during interglacial periods
(Figure 2b; Graham et al., 2003). During the LGM, sea levels were
on average about 120 m lower than today (Lambeck et al., 2002),
resulting in the broadening of coastlines and the emergence of shal-
low seabed in temperate regions (Graham et al., 2003), in some cases
creating land- bridges or continuous shallow- water habitat between
nearby landmasses. Such environmental fluctuations in temperate
coastal zones have left various genetic impacts on contemporary
coastal populations depending on the physical characteristics of
habitats and life history features of species.
Repeated shifts in the ecosystems of temperate paleo- shorelines
can explain disjunct genetic patterns in some continuously distrib-
uted coastal species (Figure 2b). MtDNA sequences of the obligate
rocky shore fish Clinus cottoides, integrated with glacial sea- level re-
constructions for the southern coastline of Africa, have shown that
rocky shores were separated by sandy beaches due to lowered sea
levels during glaciations (Toms et al., 20 14). These habitat breaks
apparently separated populations of C. cottoides in distinct rocky in-
tertidal refugia and resulted in the emergence of mtDNA phylogeo-
graphic breaks along a coastline lacking contemporary geographic
barriers to gene flow (Toms et al., 2014). Similarly, continuous fluctu-
ations in size and distribution of rocky and sandy coasts of southern
California have affected the historical continuity of coastal popu-
lations (Graham et al., 2003) and left contrasting phylogeographic
patterns in sandy versus rocky species (e.g., supralittoral isopods,
Hurtado et al., 2013). Studies on hard- bottom invertebrates of tem-
perate coasts of Atlantic Patagonia have also shown that sea- level
regression reduced suitable hard substrate habitats and led to an
increase in sandy environments over the entire Atlantic Continental
Shelf, resulting in the drastic reduction of suitable habitats and
loss of genetic diversity in rocky- shore species (de Aranzamendi
et al., 2014; Fernández Iriarte et al., 2020; Ponce et al., 2011).
The topography of the continental shelf had a major influence
on the patterns of coastal population persistence and demographic
changes during periods of sea level regression. Comparison of con-
temporary and LGM shallow seabed in southern Australia (central
and western parts of the Great Southern Reef) have shown that
more shallow- water habitats were available along wide- shelf regions
compared to narrow- shelf regions during the LGM lowstand (Stiller
et al., 2021). According to these topographic differences, the amount
of shallow seabed habitats that were gained during postglacial sea
level rise differed among different coasts and resulted in contrast-
ing regional genetic patterns and demographic responses across the
distribution range of the shallow- water leafy sea dragon, Phycodurus
eques in southern Australia (Stiller et al., 2021). Similarly, estuaries
were significantly affected by glacial sea level change because the
formation of these habitats requires specific geomorphic settings
such as low- gradient slope and a relatively broad continental shelf
(Dolby et al., 2018; Graham et al., 2003). Reconstruction of estua-
rine paleohabitat distributions in southern California has shown that
when sea level dropped to approximately 130 m during the LGM,
paleo- shorelines became too steep and narrow for the formation of
tidal estuaries, limiting these habitats to scattered wide- shelf areas
(Dolby et al., 2016, 2018). Such changes in the distribution of estua-
rine habitats restricted the LGM distribution of tidal estuarine fishes
along southern California, driving higher microsatellite allelic richness
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Parvizi et al .
and genetic connectivity in populations along broad coasts compared
to the lower allelic richness and genetically highly differentiated pop-
ulations along steep paleo- shorelines (Dolby et al., 2016, 2018).
Marine regressions during glacial episodes led to the isolation of
several temperate coastal basins. The warm- temperate coasts of the
Asian Northwest Pacific are perfect examples for understanding the
genetic impacts of glacial- driven sea level falls and basin isolation on
coastal populations. In this region, sea levels dropped to 120– 140 m
below the present levels, created enclosed marginal basins in the Sea
of Japan and eradicated suitable substrates for the survival of inter-
tidal populations in the East and South China seas (Hu et al., 2015;
Wang, 1999). The genetic impact of these habitat fragmentations is
reflected in species inhibiting shallow coastal waters such as the red
algae Chondrus ocellatus (Hu et al., 2015), the redlip mullet Chelon
haematocheilus (Liu et al., 2007) and mitten crabs Eriocheir spp. (Xu
et al., 2009) which show strong mtDNA genetic breaks between the
three marginal seas of the North- western Pacific.
Apart from affecting habitat availability and suitability, sea level
changes during the LGM significantly influenced the dispersal pattern
of warm- temperate coastal taxa, especially poor dispersers, in broad
geographic scales. The emergence of land bridges created temporary
corridors for gene flow in some species while restricting effective
migration in others. For instance, glacial sea regression is inferred to
have enabled genetic connectivity of populations of some poorly-
dispersive coastal saltmarsh plants (Suaeda spp.) of Korea and Japan
(Park et al., 2019, 2020). However, the emergence of land bridges did
not work in favour of some sea- dispersed coastal plant species. For
mangroves, the presence of large land barriers apparently restricted
Pleistocene dispersal, resulting in broad- scale phylogeographic differ-
entiation among many populations (e.g. Banerjee et al., 2020; Ya ng
et al., 2017). As a case in point, comparative genomic data from five
mangrove species in the Strait of Malacca revealed that past fluctu-
ations in sea- levels led to episodic isolation and gene flow across the
Strait, perhaps facilitating speciation with gene flow between Pacific
and Indian Ocean lineages (He & Silliman, 2019).
7 | HOW GENETIC MARKER CHOICE CAN
AFFECT RECONSTRUCTIONS OF COASTAL
DISTURBANCE DYNAMICS
A variety of molecular markers have been used in coastal phylo-
geographic studies, providing contrasting depths of insight into mi-
croevolutionary and demographic responses to disturbance history
(Figure 3). It has become increasingly clear that reliance on low num-
bers of loci leads to the underestimation of the genetic structure
and diversity (Hodel et al., 2017) and inaccurate demographic re-
constructions (Zhang & Hewitt, 2003). If inferences are solely based
on organellar DNA, for instance, the resulting phylogeographic
reconstructions may misrepresent population history due to pro-
cesses such as natural selection (Bazin et al., 2006; but see Mulligan
et al., 2006) and introgression (Chan & Levin, 2005). These effects
can be especially problematic when studying neutral processes such
as range expansion, dispersal, recolonization and recent population
history (Edwards et al., 2015; Excoffier & Ray, 2008), all of which
are the major demographic events constantly happening in marginal
marine habitats.
Data from organellar and microsatellite loci have assisted our
understanding of the broad demographic consequences of coastal
disturbances by revealing signatures of population expansion and
turnover (Figure 3). However, the use of genome- wide SNP data in
coastal phylogeography has been shown to resolve finer- scale spa-
tial patterns, and higher- resolution demographic histories relative
to those from traditional molecular approaches. Importantly, reli-
ance on small numbers of loci can result in inaccurate estimates of
population structure and gene- flow (Figure 3a,b), and obscure the
assignment of organisms to their natal regions (Figure 3c), particu-
larly in highly dispersive taxa. The increasing affordability and ease
of SNP data collection, coupled with their high information content,
and potential for accommodating assumptions of linkage and marker
independence, makes SNPs essential tools for molecular ecology
and evolution (Leaché & Oaks, 2017; Reit zel et al., 2013). Crucially,
SNPs can offer more precision in estimating population genetic pa-
rameters such as the time and magnitude of population size change
or migration rates (Leaché & Oaks, 2017) which are essential in the
context of disturbance phylogeography. Additionally, SNPs can yield
finer- scale inferences about the locations of historic refugia and
past expansion dynamics, and thus potentially indicate local phys-
ical anomalies in heterogeneous coastal habitats. Genomic data are
also highly informative for testing phylogeographic scenarios using
powerful model selection approaches such as approximate Bayesian
computation (Cornuet et al., 2014; Xue & Hickerson, 2017) and ma-
chine learning (Collin et al., 2021; Fonseca et al., 2021). Using high-
resolution genomic data, coastal phylogeographic scenarios can be
explicitly formulated and informed using geo- climatic evidence to
test alternative divergence, dispersal and colonization hypotheses.
Harnessing the power of genomic data in coastal phylogeography
can thus help us to better understand how Earth's physical pro-
cesses control diversification at such transition zones.
8 | BIOGEOGRAPHIC IMPLICATIONS OF
COASTAL DISTURBANCE
8.1 | Coastal physical controls of vicariance and
isolation
Some coastal physical processes can promote vicariance by creat-
ing physical barriers isolating adjacent coastal habitats. The cur-
rent synthesis demonstrates that historical sea- level regressions at
non- glaciated coasts have apparently been major drivers of coastal
vicariance. The physical mechanisms by which such geographic
subdivisions can occur include sea- level falls and subsequent al-
terations of coastal habitat configuration (e.g. from rocky shores to
sandy beaches) or the emergence of land bridges and basin isolation.
Specifically, historical coastal vicariance events driven by sea- level
8
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Parvi zi et al.
FIGURE 3 Recent coastal genomic studies suggest that genome- wide data can better reveal signatures of both past habitat perturbations
and contemporary physical dynamics (a) Seven microsatellites in the leafy seadragon, Phycodurus eques detected two main genetic clusters
in southern Australia, with overall low genetic diversity and evidence of postglacial colonization (Stiller et al., 2017). Using 2845 SNPs and
incorporating palaeoshoreline models, however, it was revealed that regionally different continental shelf topographies drove contrasting
patterns of genomic diversity and structure along the studied coastlines. SNPs were used in phylogeographic scenarios to test how the
width of the continental shelf during the Pleistocene sea- level regressions affected demography of populations (Stiller et al., 2021). (b)
mtDNA COI sequences revealed genetic spatial “anomalies” associated with prehistorically uplifted coast in the intertidal kelp, Durvillaea
antarctica as a result of an earthquake that happened approximately 1000 y BP in New Zealand (Parvizi et al., 2 019). Subsequently, 9710
SNPs revealed fine- scale spatial patterns and were used to test recolonization scenarios with regard to the coastal uplift zone (Parvizi
et al., 2020). (c) mtDNA COI (and other nuclear and organellar markers) of D. antarctica from sub- Antarctic islands showed near- absolute
genetic homogeneity over vast distances and indicated the LGM sea ice boundaries (Fraser et al., 2009). Later, 15,994 SNPs revealed
fine- scale population structure that could not be detected by more traditional methods, enabling researchers to pinpoint the sources of D.
antarctica rafts reaching Antarctic shores as a result of contemporary storm- forced surface waves (Fraser, Morrison, et al., 2018).
|
9
Parvizi et al .
falls are one of the underlying causes of phylogeographic breaks
along coastlines without obvious contemporary barriers to gene-
flow (e.g., Toms et al., 2014; Xu et al., 2009).
The isolation of coastal populations can also be controlled by
the difference in regional topology of the continental shelf— an im-
portant factor in constraining population connectivity during marine
regression periods. These differences can increase the isolation of
populations along narrow margins into scattered refugia and con-
sequently promote regional genetic differentiation and species
richness in these areas compared to broader shelves (e.g., Dolby
et al., 2018, 2020). Finally, coastal isolation can also occur following
earthquakes. Tectonically disturbed populations can be isolated in
uplifted habitats and thus diverge allopatrically from their coastal
ancestors (e.g., Lescak et al., 2015).
8.2 | Coastal physical controls of dispersal and
colonization
The current review highlights that a variety of disturbance- related
processes can shape dispersal patterns in coastal populations.
Generally, physical disturbances that intensify abiotic dispersal vec-
tors such as winds and currents can enhance the passive dispersal
of individuals. Long- distance transportation of individuals can be
promoted by tsunamis and hurricanes (e.g. Apodaca et al., 2013;
Brante et al., 2019; Gillespie et al., 2012; Pagán et al., 2020) and dis-
ruption to common dispersal routes can occur as a result of severe
storm events, especially in species with high buoyancy (e.g. Fraser,
Morrison, et al., 2018; Waters et al., 2018). Phylogeographic conse-
quences of such changes in coastal dispersal patterns can include
regional genetic homogeneity, increased chance of range shifts and
potentially biological invasions in marginal marine habitats.
Colonization processes in coastal habitats can be controlled by
those physical events that create new habitats or empty the pre-
viously occupied habitats. The emergence of new coastal habitats
can be the result of tectonic disturbances such as co- seismic coastal
uplifts (e.g. Parvizi et al., 2020) or landslides (e.g. Vaux et al., 2021),
hydrological processes such as tsunami (e.g. creating new sandbars,
Ohbayashi et al., 2017), or postglacial processes such as retreating
sea ice (e.g. Fraser et al., 2009; Maggs et al., 2008). Als o, coastal spe-
cies can experience local extinction and subsequent recolonization
as a result of sudden thermal stress and heatwaves. Overall, biogeo-
graphic consequences of disturbance- driven coastal colonization
can vary from striking spatial genetic sectoring, and genetic drift,
through to major species range shifts.
9 | THE SPATIAL AND TEMPORAL SCALE
OF COASTAL PHYSICAL DISTURBANCE
Physical processes at the land- sea interface can affect coastal biota
across a wide variety of temporal and spatial scales. Tectonic or at-
mospheric (such as storms) disruptions typically act over relatively
small spatial scales (e.g. mesoscale) and primarily affect communities
immediately adjacent to the epicentre of disturbance. In such cases
where only a limited number of habitats are disturbed, recovery can
potentially occur within a few generations, especially for taxa with
strong larval / rafting dispersal (e.g. Barber et al., 2002; Becheler
et al., 2020; Parvizi et al., 2020). Additionally, any genetic structure
generated by such events is likely to be extremely shallow (Parvizi
et al., 2022). The magnitude of mesoscale disturbances can control
the rate at which spatial struc ture develops, with larger, more destruc-
tive disturbances resulting in faster fixation of haplotypes and rapid
restructuring of spatial genetic patterns (Fraser, Davies, et al., 2018). In
some cases, mesoscale disturbances can be compounded by additional
ecological stressors (e.g. grazers supressing kelp recovery following
marine heatwaves, McPherson et al., 2021; low water clarity increas-
ing temperature- induced kelp loss, Tait et al., 2021). Co- occurring dis-
turbances can have particularly strong consequences for coastal biota
(e.g. the cascading impacts of earthquakes and marine heatwaves on
bull kelp communities, Thomsen et al., 2021). In such cases, the cumu-
lative effects of concerted mesoscale catastrophic events can exacer-
bate the intensity and duration of regional disturbances and result in
long- lasting evolutionary shifts in disturbed locations.
In contrast to mesoscale events (above), major climate- driven
disturbances such as glaciations and sea- level changes typically
operate over vast geographic scales and extended time spans (e.g.
Lau et al., 2020; Maggs et al., 2008), with associated ecosystem
change or recovery representing an extended process (Hofreiter &
Stewart, 2009). From an evolutionary perspective, such large- scale
disturbances can generate relatively deep phylogenetic divergences,
sometimes resulting in concordant speciation patterns across sev-
eral codistributed marine taxa (Bowen et al., 2016). Interestingly, de-
spite considerable research effort over several decades, some of the
more nuanced biological impacts of global coastal disturbance are
only now coming to light via the integration of spatial models with
genome- wide data (e.g. Stiller et al., 2021).
10 | CONCLUSIONS: FUTURE
INTEGRATION OF COASTAL GENOMIC AND
PH YSIC A L DATA
Broadly, genomic studies are changing our understanding of coastal
ecosystems. Although many previous studies have considered
long- lived climatic fluctuations to be primary drivers of marine
biodiversity patterns (e.g. Bowen et al., 2016; Fraser et al., 2009;
Maggs et al., 2008), emerging dat a highlight that a variety of rela-
tively short- lived disturbances can similarly underpin major coastal
biological shifts. Notably, recent genetic studies highlight the on-
going biogeographic roles of storm events on coastal populations,
with implications for both diversity and distributions (e.g. Gillespie
et al., 2012). Indeed, as such atmospheric disr uptio n events are argu-
ably a defining characteristic of many coastal systems, disturbance-
related phylogeographic processes should perhaps similarly be seen
here as the rule more than the exception. Along similar lines, recent
10
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Parvi zi et al.
studies reveal the pervasive coastal biological effects of geological
disturbance in tectonically active regions of the globe (reviewed in
Thomsen et al., 2021). For instance, the 1964 Alaskan earthquake
which initiated rapid speciation in sticklebacks (Lescak et al., 2015)
also eliminated numerous populations of seagrass, Zostera marina
(Short & Wyllie- Echeverria, 1996). Such disturbance- impacted
coastal systems clearly provide strong opportunities for future mul-
tispecies genomic analysis.
Based on our synthesis, we suggest that future coastal genomic
studies should seek to better account for the impacts of ephemeral
disturbance processes. Consideration of detailed disturbance history
should help to inform hypothesis development, and also influence the
study design (e.g. geographic site selection and sampling strategies).
In coastal zones that are particularly prone to short- term mesoscale
disturbance, for example, temporal comparisons of pre- and post-
disturbance samples should facilitate the identification of disturbance
impacts, which may oth erwise be difficult to detect fro m moder n sam-
ples alone. Additionally, the impacts of abiotic stressors can poten-
tially be identified using experimental evolutionary approaches (see
Kelly & Griffiths, 2021), with implications for predicting effects of al-
tered disturbance regimes under future climatic scenarios.
Overall, our synthesis highlights that coastal phylogeographic
patterns are heavily influenced by disturbance over a vast range of
spatiotemporal scales, including long- lived processes that reshape
coastal landscapes globally (e.g. historical glaciations), and short- term
disturbances impacting coastal populations at local scales (e.g. sudden
atmospheric and tectonic events). Additionally, as biotic / life- history
trai ts (e.g. ha bit at choice and dis per sal capaci ty) may str ongly inf lue nce
species- specific responses to disturbance, multispecies approaches are
needed to account for such biological variability (Parvizi et al., 2022).
In particular, multispecies approaches combining genome- wide se-
quencing and paleoenvironmental data (e.g. Paleo- MARSPEC data lay-
ers; Sbrocco, 2014) hold promise for elucidating how disturbance can
shape coastal biodiversity patterns (Dolby et al., 2022). Specifically,
a geo- genomic approach is fundamental for identifying the regional
topographic features of coastal zones that can buffer populations
against different types of disturbance, and/or for testing the role of
ongoing short- term disturbance on coastal biotic evolution.
Broadly, multispecies phylogeographic analysis from disturbance-
prone regions has potential to reveal trait- specific impacts of distur-
bance (e.g. Parvizi et al., 2022). Comparative genomic approaches
coupled with mode l- based tes ts (see Section 7) can elucidate the ex-
tent to which deeper- time or short- term physical disruptions struc-
ture coastal biodiversity. Disturbance of habitat- forming coastal
taxa (e.g. kelp forests, seagrass beds, coral reefs, all of which support
facilitative species interactions [Bruno et al., 2003]) can potentially
affect vast numbers of associated species with disparate ecological
traits, and comparative population genomics provides a particularly
powerful tool to identify idiosyncratic responses to disturbance.
Because the magnitude and frequency of natural disturbances is
increasing (Kerr, 2011; Wernberg et al., 2013), such insights are es-
sential for exploring the future evolutionary capacity of populations
inhabiting the dynamic land- sea interface.
ACKNOWLEDGEMENTS
This study was supported by the Marsden Fund administered by
Royal Society of New Zealand (UOO1818) awarded to J.M.W., the
Rutherford Fellowship grant (UOO1803) awarded to C.I.F. and an
Otago PhD Scholarship awarded to E.P. No specific permits were
needed to carry out this study.
CONFLICT OF INTEREST
We declare no conflict of interest.
DATA AVA ILAB ILITY STATE MEN T
No new data were created or analysed as part of this synthesis
article.
ORCID
Elahe Parvizi https://orcid.org/0000-0002-1695-8817
Ceridwen I. Fraser https://orcid.org/0000-0002-6918-8959
Jonathan M. Waters https://orcid.org/0000-0002-1514-7916
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BIOSKETCH
This Synthesis constitutes the final chapter of Elahe Parvizi's PhD
thesis on the phylogeographic impacts of a prehistoric coastal
uplift in New Zealand. The authors share research interests in
how earth's physical processes affect genomic patterns and de-
mographic histor y of marine taxa.
Author contributions: All au thors contributed equally to the co n-
ceptualization of the study. E.P. prepared the original draft. All
authors reviewed and edited the manuscript.
How to cite this article: Parvizi, E., Fraser, C. I., & Waters, J.
M. (2022). Genetic impacts of physical disturbance processes
in coastal marine ecosystems. Journal of Biogeography, 00,
1–14 . https://doi.org /10.1111/jbi.14464
