Marine Biology (2021) 168:105

https://doi.org/10.1007/s00227-021-03891-2

ORIGINAL PAPER

Demographic history, not larval dispersal potential, explains

differences in population structure of two New Zealand intertidal
species
Vanessa Arranz1,2,3 · Vibha Thakur1 · Shane D. Lavery1,2

Received: 30 March 2020 / Accepted: 20 April 2021 / Published online: 19 June 2021
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021

Abstract
Two unresolved questions in marine population connectivity are: (1) the relative importance of contemporary and histori-
cal factors (e.g., ongoing gene flow versus past demographic events), and (2) to what extent species subject to the same
evolutionary forces exhibit similar phylogeographic patterns. Here, we address these questions using two species from New
Zealand’s rocky shore that have very similar distributions and life histories, but very different larval dispersal abilities: the
cat’s eye snail Lunella smaragda has short-lived pelagic larvae (3–4 days) while the half-crab Petrolisthes elongatus has
a longer pelagic larval duration (3–4 weeks). A large number of individuals of these species were collected (n = 727 and
440) at different locations (31 and 20) throughout their wide New Zealand distribution. These species were analysed for
both mitochondrial DNA cytochrome oxidase I (COI) and nuclear ribosomal internal transcribed spacer (ITS-1) variation.
Contrary to expectations, the species with much greater dispersal potential, P. elongatus, exhibited much greater population
differentiation (> fivefold for mtDNA ΦST, > 50-fold for nDNA ΦST). This study highlights that species along the same coast
can show remarkably different patterns of population structure, and that although there appear to be some common geographic
discontinuities in New Zealand, there are few common overall patterns that apply to many species. The study reinforces the
observation that predictions of population structure based on life history are often not upheld, and shows that differences in
demographic history may be an important factor in driving contemporary patterns of genetic diversity.

Introduction are influenced by the same evolutionary forces to produce

There are many unresolved questions in our understanding
of the population structure and connectivity within marine
species (Brown et al. 2016). One of those is what is the
relative importance of contemporary and historical factors
in driving the genetic patterns seen today. Another is the
degree to which species in the same region and community
Responsible Editor: M. Rius.
Reviewed by: C. Carreras and A. McGaughran.
* Vanessa Arranz
vanearranz@hotmail.com
1
School of Biological Sciences, University of Auckland,
Private Bag 92019, Auckland 1142, New Zealand
2
Institute of Marine Science, University of Auckland, Private
Bag 92019, Auckland 1142, New Zealand
3
School of Natural and Computational Sciences, Massey
University Auckland, Albany, Auckland 0745, New Zealand
similar genetic patterns throughout their geographic ranges
(Avise 2000). A valuable method of addressing both these
questions is to compare the spatial genetic structure of a
variety of species from the same community, “comparative
phylogeography” (Avise et al. 1987; Avise 2000), to tease
apart the importance of common or species-specific factors
in driving the spatial evolution of marine communities.
A valuable environment in which to explore these fac-
tors is the New Zealand coastline. The marine communities
here are diverse, geographically isolated, largely endemic
and have been the subject of a long history of population
genetic studies (Ross et al. 2009), which enables a rela-
tively comprehensive comparison of interspecific patterns
of population structure. Overviews of New Zealand marine
coastal connectivity have, to date, highlighted the impor-
tance of present-day forces (e.g. coastal currents) in restrict-
ing larval dispersal, but have not been able to make strong
conclusions about the importance of species-specific larval
dispersal ability in determining differences in genetic pat-
terns (Ross et al. 2009). The pelagic larval duration, PLD,

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is often used as a proxy for larval dispersal, and its correla-
tion with marine population structure has been extensively
studied, but there are contradictory interpretations of the
relationship, with no clear resolution (e.g., Galarza et al.
2009; Riginos et al. 2011; Selkoe and Toonen 2011; Pas-
cual et al. 2017).
Previous overviews of New Zealand coastal marine con-
nectivity have concluded that several different spatial genetic
patterns are evident across a range of species. A number of
studies have revealed the existence of a common genetic
discontinuity between northern and southern regions in
many taxa. The location of the discontinuity has been placed
near the north end of the South Island in some species but
does not appear to be the same across taxa (Supplemen-
tary Table S1). Not all studies have reported a north–south
genetic discontinuity, and several other patterns have been
found, including the absence of genetic structure (panmixia),
which, not surprisingly, has been described in species with
very long PLD (Brasher et al. 1992; Ovenden et al. 1992).
Another genetic pattern frequently found is isolation-by-dis-
tance (IBD) (Hickey et al. 2009; Veale and Lavery 2012). A
final common pattern is east–west differentiation between
the two coasts of the North Island (Stevens and Hogg 2004;
Veale and Lavery 2011).
A range of explanations have been put forward to explain
the processes behind these common genetic patterns in New
Zealand waters. Those explanations have been dominated by
the impacts of present-day forces, such as coastal currents
and upwelling, on dispersal and gene flow (Apte and Gard-
ner 2002; Veale and Lavery 2011). However, there has not
previously been a strong emphasis on examining the impact
of past demographic events on population connectivity in
New Zealand, which has been shown to have a strong effect
in other geographic regions (McGovern et al. 2010; Marko
and Hart 2011).
The study presented here compared the patterns of gene
flow between populations of two of the most common,
endemic, benthic intertidal species in New Zealand, tested
whether they matched previously described patterns of
population structure, and examined the potential impact of
their past demography. The cat’s eye snail, Lunella smar-
agda (Gmelin, 1791) and the half-crab, Petrolisthes elon-
gatus (H. Milne-Edwards, 1837) are found in very similar
intertidal environments and are both commonly found along
much of the coastline around New Zealand, thus enabling
the most extensive comparative sampling possible. However,
even though both species experience very similar physical
environments, and have many similar life history parameters,
they have very different modes of larval dispersal.
L. smaragda (Family Turbinidae) is a broadcast spawner
with external fertilisation. It has a short spawning season
at the end of summer, between February and April, and
settlement of the larvae probably occurs within 3–4 days
13
Marine Biology (2021) 168:105
after fertilisation (Grange 1976). This short pelagic larval
phase and short spawning season significantly restrict the
dispersal ability and potential gene flow. Consequently,
it was expected that this species would exhibit relatively
higher levels of population subdivision. P. elongatus (Fam-
ily Porcellanidae) has pelagic larvae that can survive in the
water column between 12 days (Fujita and Osawa 2005)
and 30 days (Saelzer et al. 1986) and, under experimental
conditions, over 100 days (MacMillan 1972). The breed-
ing season decreases in duration with increasing latitude
(McLay 1988), from 12 months at Auckland in the north
(Greenwood 1965) to 9 months at Wellington (Wear 1965)
and 6 months at Kaikoura in the South Island (Jones 1977).
Despite their taxonomic differences, most other critical life
history parameters are very similar between the two species.
Both species disperse only during the pelagic larval phase,
have summer breeding seasons, similar lifespans, similar
reproductive output, and no sex bias (Walsby 1977; McLay
1988). The only major differences are the far longer PLD
and spawning season in P. elongatus, which both create con-
siderably greater dispersal potential that could allow genetic
admixture between distant populations (McLay 1988). The
expectation is for a considerably greater population genetic
structure within L. smaragda due to its much more limited
dispersal potential.
This study aimed to: (1) Compare population connectiv-
ity between two co-occurring benthic marine invertebrates
that differ dramatically in PLD, over a broad geographic
scale (New Zealand-wide), (2) assess if the patterns of gene
flow within these species coincide with previously described
common genetic boundaries and (3) investigate the demo-
graphic histories of the species to uncover their potential
importance in explaining the present population structure.
Methods
Sampling collection and DNA extraction
Specimens of L. smaragda and P. elongatus were collected
from intertidal rocky reefs at 31 and 20 localities, respec-
tively (Table 1 and Supplementary material Fig. S1). Col-
lections were made over the period 2013–2017, but the great
bulk of collections were made 2014–2015. Between 3 and
50 specimens were collected per locality, immediately pre-
served in absolute ethanol, and stored at 4 °C. Total DNA
was extracted using Qiagen’s DNEasy® Blood and Tissue
Kit. PCR amplifications in a PCR System 9700 thermal
cycler (Applied Biosystems) and Sanger sequencing of the
mitochondrial DNA cytochrome oxidase I (COI) and nuclear
ribosomal internal transcribed spacer (ITS-1) followed PCR
protocols and programmes detailed in Supplementary Mate-
rial, Table S2. All individuals were analysed for COI, while
Marine Biology (2021) 168:105 Page 3 of 14 105

Table 1  Population Population Population code Year collected Sample size (mtDNA/nDNA)
location and sample size
for Lunella smaragda and Lunella smaragda Petrolis-
Petrolisthes elongatus. thes
Populations are ordered in a elongatus
clockwise direction around
the New Zealand coast. All North Island
populations above the dotted Taranaki TAR​ 2015 23/– 20/32
line are situated in the North Raglan RGL 2014 32/–
Island and sites below in the
South Island Mosquito Beach WES 2015 18/14 28/30
Ahipara AHI 2015 17/–
Cape Reinga CPR 2015 24/28
Taupo Bay TAB 2014 23/–
Mimiwhanghata MIM 2013 53/–
Tawharanui Regional Park MAO 2016 23/30 26/–
Whangaparaoa Peninsula WHG 2014 22/–
Great Barrier Island GBI 2013 22/48 22/26
Orewa ORE 2014 20/–
Devonport DEV 2015 18/– 24/–
Saint Heliers STH 2015 21/14 24/–
Waiheke Island WHK 2015 2/–
Coromandel COR 2015 24/– 22/36
Waihi Beach WAB 2014 24/16
Waihau Bay ECA 2014 25/– 25/–
Gisborne GIS 2015 33/18 25/32
Hawkes Bay HWB 2016 19/– 24/–
Cook Strait
Lyall Bay LYA 2016 19/–
Makara Beach MAK 2016 13/– 9/–
Pukerua Bay PUK 2015 29/20
Wharariki Beach WHA 2015 29/–
Kaiteriteri KAT 2015 36/24 18/–
Okiwi Bay, Malborough OKI 2015 28/– 21/30
South Island
Picton PIC 2015 26/–
Kaikoura KAI 2015 34/– 6/–
Christchurch CHC 2015 3/– 20/28
Dunedin DUN 2015 28/22 30/32
Slope Point, The Catlins SLO 2015 28/32 25/-
Oban, Stewart Island STE 2015 3/– 26/28
Jackson Bay, West Coast JAC 2015 26/24 23/26
Total samples 727/145 440/150

for ITS-1, a subset of individuals was selected that repre-
sented the geographic and genetic diversity (Table 1).
Data analysis/population genetic analyses
All sequences were edited and aligned using Geneious®
v. 9.1.6 (Kearse et al. 2012) and the results from the
alignment verified by eye. Sequences of the haplotypes
found in this study were deposited in GenBank (see Avail-
ability of data and material section). ITS-1 haplotypes
showed low polymorphism, and heterozygote haplotypes
were easily phased manually, and confirmed using the
programme PHASE (Stephens and Donnelly 2003).

13
105 Page 4 of 14
Genetic diversity
Number of haplotypes (Nh), number of private haplotypes
(Np), nucleotide diversity (π), haplotype diversity (Hd) for
the COI region and expected (He) and observed (Ho) het-
erozygosity (Nei 1978) for the ITS region and values were
calculated, for each location and for both islands in both spe-
cies, using ARLEQUIN v. 3.5 (Excoffier and Lischer 2010)
and DnaSP v. 5.10 (Librado and Rozas 2009).
The complete data sets of mitochondrial and ITS
sequences were used to construct unrooted networks for
each species using Network v. 5.0.0.0 (Bandelt et al. 1999).
To simplify interpretation of the spatial structure, haplotype
origins were grouped into three regions (North, South and
Cook Strait see Table 1).
Population differentiation
Analysis of population differentiation was assessed with
both genes. Pairwise genetic divergences between popu-
lations were calculated based on haplotype frequencies
(standard ­FST), on genetic distances between haplotypes
using Kimura 2-parameter corrected measure (Kimura
1980) (ΦST) and on Slatkin’s standardised pairwise FST value
[FST/(1 − FST)] (Slatkin 1993). Significances were tested
with 10,000 permutations in ARLEQUIN v. 3.5 (Excoffier
and Lischer 2010). The B–Y false discovery rate (FDR)
method was used to adjust significance levels for multiple
tests. Locations with less than N = 3 were excluded from the
analysis to avoid poor representation. Principal Coordinates
Analysis (PCoA) was performed with Genalex v. 6. (Peakall
and Smouse 2012) to graphically visualise interrelationships
represented by the matrix of population pairwise genetic dif-
ferentiation. Genetic variation within and among geographic
groups was studied through analyses of the molecular vari-
ance (AMOVA) using haplotype frequencies (FST) and
matrices of genetic distances (ΦST) in both species. Popu-
lations were grouped according to different criteria to test
where the major genetic differentiation occurred: (1) North
vs. South Island, (2) North Island + Cook Strait populations
of South Island; vs. remainder of South Island (see Table 1)
and (3) adjacent sample populations grouped in a manner
that maximised the difference between geographic regions
and minimised the variability within regions. The first two
criteria were based on a priori predictions from previous
studies (Ross et al. 2009), while the third attempted to cap-
ture the major spatial genetic divergences evident in the data.
This last sample population grouping was based on the con-
cordance of results from spatial analyses conducted using
AMOVA, SAMOVA (Dupanloup et al. 2002), BAPS (Cheng
et al. 2013), PCoA, and population pairwise tests of diver-
gence in FST and ΦST; common genetic boundaries identified
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Marine Biology (2021) 168:105
by all methods were retained. Separate sample population
groupings were undertaken for the COI and ITS-1 data sets.
The potential effect of isolation by geographic distance
was assessed using the Mantel test (Mantel 1967; Rousset
1997) with 10,000 permutations with vegan (Oksanen et al.
2007) package in R (R Core Team 2019). For this, the corre-
lation of matrices of standardised pairwise genetic distances
values (Slatkin’s FST) and shortest coastal distances between
samples (km) was tested. The coastal distances were meas-
ured following the coastal geography with Google maps.
Historical demography
Departures from neutral expectations were examined to shed
light on demographic history. This was first studied with
tests of neutrality such as Fu’s FS (Fu 1997) and Tajima’s D
(Stanton 1973; Tajima 1989) obtained with DnaSP v. 5.10
(Librado and Rozas 2009) using the mitochondrial locus.
The fit of the mismatch distributions to the expected distri-
butions in an expansion scenario was also tested. Mismatch
distribution statistics (Tau (T), sum of squares deviation
(SSD) and probabilities (p)) were calculated in ARLEQUIN
v. 3.5. The test was performed for each site, the whole data-
set and the significantly different geographic groups iden-
tified in previous analyses. The time of a possible expan-
sion was assessed using the relation τ = 2 ut (Rogers and
Harpending 1992), where t is the time in generations, using
1 generation per year, τ was the median of the mismatch
distribution, and u the substitution rate.
For the same differentiated groups and the whole species
COI datasets, the past changes in population size and times
of expansion were estimated by generating Bayesian Skyline
Plots (BSP), a model-free coalescent-based method imple-
mented in the software BEAST v. 2.4.2 (Drummond and
Rambaut 2007). The best-fit models of nucleotide substitu-
tion for each species data set were selected with jModeltest
v. 3.06 (Posada and Crandall 1998) under AIC and BIC cri-
terion. The most reliable estimates available of substitution
rate within each species were obtained from the literature,
although recognising that short-term population substitution
rates are likely to be higher (Ho et al. 2011). The substitution
rate estimate for L. smaragda was 2.4% per MY (1.2% per
lineage per MY), based on a recent 3.2 MY species diver-
gence in a confidently dated COI phylogenetic analysis of
the genus Lunella by Williams et al. (2011) and a phylogeo-
graphic study from the closely related L. granulata (Chiu
et al. 2013). The substitution rate estimate for P. elongatus
was 1.4% per MY (0.7% per lineage), based on the recent
3 MY species divergence in a confidently dated phylogeo-
graphic analysis of the closely related P. armatus, also using
the same COI fragment (Hiller and Lessios 2017). Both of
these estimates correlate strongly with those of recent esti-
mates from other related mollusc and crustacean lineages.
Marine Biology (2021) 168:105
Results
Genetic diversity
A total of 727 and 440 sequences of a partial fragment of
586 bp and 605 bp of the COI region were obtained for
L. smaragda and P. elongatus, respectively. P. elongatus
showed higher haplotype diversity (h) than L. smaragda
(0.918 and 0.463, respectively). Even though the nucleo-
tide diversity (π) was relatively low in both species, it was
lower in L. smaragda (0.0013) than in P. elongatus (0.0069).
For L. smaragda, both diversity indices were significantly
higher in the North Is. (h = 0.563, π = 0.17%) compared to
the South Is. (h = 0.226, π < 0.05%), while this differential
pattern was not shown in P. elongatus (Supplementary mate-
rial, Table S3).
For the nuclear marker, 145 and 150 sequences of a
fragment of 548 bp and 318 bp from the ITS-1 region,
were obtained for L. smaragda and P. elongatus, respec-
tively. Overall nucleotide diversity indices were low in
both species (P. elongatus 0.1%, and L. smaragda 0.3%).
Total observed heterozygosity was low and similar in
both species (L. smaragda 0.054 and P. elongatus 0.062).
L. smaragda exhibited similar values of heterozygosity
Fig. 1  Haplotype networks for Lunella smaragda and Petrolisthes
elongatus. Left figures correspond with mtDNA (COI), right nDNA
(ITS-1). Every haplotype is separate by one mutational step; those
Page 5 of 14 105
in North (0.063) and South Island (0.080). However,
P.elongatus showed higher heterozygosity in South Is.
populations (0.155) than North Is. (0.046) (Supplemen-
tary material Table S3).
The COI haplotype network of L. smaragda had a sim-
ple star shape, with one common haplotype and many
low-frequency haplotypes separated by one or few muta-
tional steps from the common haplotype (Fig. 1). The
network revealed little phylogeographic structure. One
notable result was the existence of a rare haplotype found
almost exclusively on Great Barrier Island (GBI), where
it occurred in 50% of individuals. The ITS-1 network also
had a similar star shape, with only single step mutations
between alleles, and little phylogeographic structure. No
private ITS-1 haplotype was recorded on GBI.
The P. elongatus COI network had much greater phylo-
geographic structure, with several middle frequency hap-
lotypes, numerous privates haplotypes and haplogroups
that occurred predominantly in only one region (North I.,
Cook Strait, or South I.) (Fig. 1). There was no evidence
of a private haplotype on Great Barrier I., as was seen in
L. smaragda. The ITS-1 network exhibited considerably
lower variability in this locus, but again revealed signifi-
cant phylogeographic structure, with most common alleles
found in only one or two regions.
marked as red dots were not observed. Yellow: North Island; Green:
Cook Strait and Purple: South Island
13
105 Page 6 of 14
Population differentiation
Lunella smaragda
Lunella smaragda exhibited relatively low, but significant,
levels of population differentiation among all sampled popu-
lations, with significant differences in haplotype frequen-
cies (Supplementary Material, Fig. S2 and S3). The COI
(mtDNA) region of L. smaragda exhibited significant overall
ΦST = 0.0304 (p < 0.001). Even at the fine scale of within the
Hauraki Gulf, some differences were observed, with a rare
mtDNA haplotype occurring at high frequency in the GBI
sample, although there was no indication of ITS-1 differen-
tiation of this sample. The overall mtDNA differentiation
was ΦST = 0.0126 (p < 0.01) after excluding the anomalous
GBI sample from this analysis (see “Discussion”). The
ITS-1 region also showed relatively low levels of differen-
tiation, where the overall ΦST = 0.0032 (p = 0.297) was not
significant.
Pairwise FST values showed that most sampled popula-
tions were significantly different from each other in COI
Fig. 2  a Principal Coordinates Analysis (PCoA) plot based on pair-
wise COI ΦST values among 28 populations of Lunella smaragda.
Hauraki Gulf populations were pooled (ack). b L. smaragda PCoA
plot based on pairwise ITS-1 ΦST values among 12 locations. c PCoA
plot based on pairwise COI ΦST values among 21 populations of
13
Marine Biology (2021) 168:105
haplotype frequency, (Supplementary Material, Table S4),
while the population pairwise analysis of ΦST with the mito-
chondrial region revealed a major divergence between GBI
location and the other locations. Kaikoura (KAI) and Stew-
art Island (STE) were also distinct from other populations.
This pattern is shown in the PCoA plot of pairwise COI ΦST
values among populations (Fig. 2a). Again, most sampled
populations were significantly different from each other in
ITS-1 haplotype frequency, (FST) (Supplementary Material,
Table S5). Interestingly, the nuclear DNA ΦST did not reveal
any distinct differentiation of GBI, but instead highlighted
a significant divergence of Slope Point (SLO), which was
observed in the PCoA plot (Fig. 2b). The COI region dem-
onstrated some relationship between genetic and geographic
distance (i.e., isolation-by-distance), but only a small pro-
portion of the genetic variation was explained (r2 = 0.209,
p < 0.05) (Supplementary Material Fig. S4).
To test for the existence of a phylogeographic break
between North and South Islands, as several previously
studied species have exhibited an AMOVA was undertaken
grouping all North Island versus all South Island locations
Petrolisthes elongatus. Circle enclosing the Cook Strait populations
and Jackson point (jac). d P. elongatus PCoA plot based on pairwise
ITS-1 ΦST values among 12 locations. North Island locations are
shown in red, and South Island in blue. Population code names are
in Table 1
Marine Biology (2021) 168:105 Page 7 of 14 105

(Table 2). Due to the particularly large and anomalous dif-
ference in the GBI population shown in the L. smaragda
COI region, this location was excluded for this analysis, as
it would have biased this test. There was a significant differ-
ence between the two regions in this test (COI ΦCT = 0.0049,
p < 0.001, ITS-1 ΦCT = 0.0106, p < 0.001). Given the affinity
that northern locations of the South Island (bordering Cook
Strait) have often shown with North Island locations (Ross
et al. 2009), an additional AMOVA was performed group-
ing locations in this manner (Table 2). The results showed
an increase in the overall divergence between groups (COI
ΦCT = 0.0061, p < 0.001, ITS-1 ΦCT = 0.0230, p < 0.001).
Considering all tests of divergence, adjacent sample pop-
ulations were grouped to maximise the difference between
geographic regions and minimise the variability within
regions. Sample population grouping was based on the con-
cordance of results from spatial analyses conducted using
AMOVA, SAMOVA, BAPS, PCoA and population pair-
wise tests of divergence in FST and ΦST. As most population
comparisons were significant for FST, but only some were
significant for ΦST, this led to ΦST providing more valuable
population structure signal at the broad scale. This clustering
process on the mtDNA data divided New Zealand into seven
regions (Fig. 3a). All regions were significantly differenti-
ated from each other on haplotype frequencies (FST), but
were not all phylogeographically distinctive (ΦST) (Supple-
mentary Material Table S6). The maximally distinct regions
for the nuclear gene were broadly similar, but with slightly
different population groupings (Fig. 3b). Pairwise tests of
haplotype frequency (FST) between nDNA regions were all
significant, but the tests of ΦST were mostly not significant.
The only region that was significantly different for ΦST was
S_SI (Supplementary Material Table S7), similar to the COI
analysis.
Petrolisthes elongatus
For P. elongatus, both mtDNA and nDNA showed highly
significant differences in haplotype frequencies (Supple-
mentary Material Fig. S5 and S6), and highly significant
population differentiation based on pairwise FST and ΦST
values. The COI region showed significant overall differ-
entiation, ΦST = 0.0618 (p < 0.001). At the fine scale, there
were no significant differences among Hauraki Gulf sam-
ples, which were pooled in subsequent analyses. Based on
the ITS region, the high overall FST = 0.5304 (p < 0.001)
and ΦST = 0.1680 (p < 0.001) suggested very strong popu-
lation structure around New Zealand.
Most COI pairwise population pairwise FST values were
significant (Supplementary Material Table S8). The COI

Table 2  AMOVA from ΦST Source of variation ΦCT ΦSC ΦST

(Kimura 2P) results for Lunella mtDNA/nDNA mtDNA/nDNA mtDNA/nDNA
smaragda with mtDNA (COI)
and nDNA (ITS). Locations (a) North Island; South Island 0.0049/0.0106 0.0135/− 0.0021 0.0183/0.0084
were grouped into regions: (a)
(b) North Island 0.0061/0.0230 0.0134/− 0.0069 0.0205/0.0161
North Island and South Island,
(Whb + Kat + Oki + Pic);
(b) North Island (including
South Island
northern locations of South
Island) and South Island, (c) (c) 7 mtDNA regions 0.0295/NA 0.0087/NA 0.0380/NA
7 mtDNA regions and (d) 4 (d) 4 nDNA regions NA/0.0267 NA/0.0199 NA/0.0363
nDNA regions. Significant
values in bold

Fig. 3  a Lunella smaragda

maximally different population
groups based on mtDNA (COI).
b L. smaragda maximally dif-
ferent population groups based
on nDNA (ITS). c L. smaragda
summary map of potential
genetic barriers between four
main regional groups. Specific
locations included in each group
indicated in Supplementary
Material, Tables S4 and S5

13
105 Page 8 of 14
results for the pairwise Φ ST indicated that North Island
populations were the most homogeneous. Most of the
significant pairwise comparisons were found among the
South Island locations and between these and the North
Island populations. GBI was not differentiated, unlike in
L. smaragda. The PCoA plot (Fig. 2c) revealed the genetic
division between North and South Islands, but also showed
that populations from Cook Strait (MAK, KAT and OKI)
and western South I. (JAC) were intermediate. The results
obtained from the nuclear region are largely consistent
with the mtDNA, in that the South Island populations
(with exception of Christchurch, CHC) showed significant
pairwise difference from those in the North Island (Sup-
plementary Material Table S9). However, the ITS-1 results
exhibit little differentiation among the South I. populations
(Fig. 2d). The proportion of the genetic variance explained
by geographic distance was higher than in L. smaragda
(r2 = 0.4322, p < 0.001) (Supplementary Material Fig. S4).
An AMOVA test of COI data revealed strong and signifi-
cant genetic difference between pooled North I. versus South
I. populations (ΦCT = 0.0541, p < 0.001) (Table 3). When
the northern locations of South Island (KAT and OKI) were
Table 3  AMOVA from ΦST (Kimura 2P) results for Petrolisthes elon-
gatus with mtDNA (COI) and nDNA (ITS-1)). Locations for both
species were grouped into regions: (a) North Island and South Island,
(b) North Island (including northern locations of South Island) and
Source of variation ΦCT
mtDNA/nDNA
(a) North Island; South Island 0.0541/0.1655
(b) North I. (Whb + Kat + Oki + Pic); South I 0.0823/0.1655
(c) North I., Cook St., South I 0.0922/0.1311
(d) 6 mtDNA regions 0.0968/NA
(e) 6 nDNA regions NA/0.2450
Fig. 4  a Petrolisthes elongatus
maximally different population
groups based on mtDNA (COI).
b P. elongatus maximally dif-
ferent population groups based
on nDNA (ITS). c P. elongatus
summary map of potential
genetic barriers between four
main regional groups. Specific
locations included in each group
indicated in Supplementary
Material, Tables S8 and S9
13
Marine Biology (2021) 168:105
pooled with the North Island group, the overall differentia-
tion increased considerable to 0.0823 (p < 0.001). As the
PCoA plot revealed a third, intermediate geographic group-
ing, an AMOVA was also undertaken on the three groups
(Table 3c). This test revealed greater differentiation among
groups (ΦCT = 0.0922, p < 0.001) and lower variation among
populations within groups (ΦSC = − 0.0009, p = 0.541). This
population grouping did not improve differentiation for the
nuclear data.
All tests of population divergence were used to group
adjacent P. elongatus populations into geographic regions to
obtain the maximum difference between groups and mini-
mum within groups. Six regions were defined using the
mtDNA information (Fig. 4a). The ΦST difference among
groups was highly significant (ΦCT = 0.097, p < 0.001)
(Supplementary Material, Table S10). The regional group-
ings with the nuclear ITS-1 gene were highly differentiated
(ΦCT = 0.245, p < 0.001), and were very similar to the ones
obtained from mtDNA (Fig. 4b and Supplementary Material
Table S11). For both genes, the most significant geographic
differences were among four major regions: one cluster in
South Island and locations were also partitioned in three groups sug-
gested in MDS plot (c) North Island, Cook Strait (Mak, Kat, Oki) +
Jac and South Island, (d) 5 groups with mtDNA and (e) 6 groups with
nDNA Significant values in bold
ΦSC ΦST
mtDNA/nDNA mtDNA/nDNA
0.0246/0.0763 0.0774/0.2292
0.0166/0.0763 0.0976/0.2292
− 0.0009/0.0877 0.0912/0.2073
0.0048/NA 0.0613/NA
NA/− 0.0141 NA/0.2344
Marine Biology (2021) 168:105
the North Island, another corresponding with the Cook Strait
region, and another two in the South Island.
Summarising the tests of population differentiation across
loci for each species resulted in summary maps of the geo-
graphic locations of the greatest potential genetic barriers
(Figs. 3c and 4c). These highlight similarities in these pat-
terns between species, although the degree of differentiation
among regions was much greater in P. elongatus.
Historical demography
In L. smaragda, the star-shaped haplotype network suggests
a recent and rapid population growth, and, demographic
expansion is supported by significant negative values for
population neutrality tests in both the mitochondrial region
(Tajima’s D = − 2.653, p < 0.001; Fu’s F = − 7.520, p < 0.01)
and nDNA region (Tajima’s D = − 1.692, p < 0.001; Fu’s
F = − 14.209, p < 0.01). In addition, tests of the mismatch
distributions did not reject the null hypothesis of population
expansion (Supplementary Material Table S12). For further
analysis, the populations were broadly divided into North
Island, Cook Strait and South Island regions (see Table 1),
in line with the major genetic divergences observed, to test
whether the time of expansion differed between different
latitudinal groups. Over all populations, a Bayesian Skyline
plot (BSP) provides support for an expansion (approximately
80-fold) beginning about 40,000 years ago with a confidence
interval of 25,000–50,000 ybp. (Fig. 5). BSPs generated for
North I., South I. and Cook Strait independently, indicate
that the expansion is most well supported in the North I.
populations (Fig. 5).
In P. elongatus, although there is considerably more struc-
ture in the haplotype networks, there is also a similar pattern
Fig. 5  Bayesian skyline plots (BSP) of the effective population
size through time (in million years). Upper line corresponds to
Lunella smaragda and lower line to Petrolisthes elongatus. Each col-
Page 9 of 14 105
of high haplotype and low nucleotide diversity. Population
neutrality tests were significantly negative, predominantly in
North I., supported by both mtDNA (Tajima’s D = − 2.389,
p < 0.01; Fu’s F = − 5.745, p < 0.01) and nDNA (Tajima’s
D = − 1.472, p < 0.05; Fu’s F = − 10.141, p < 0.001). Tests
of the mismatch distributions did not reject a recent demo-
graphic expansion (Supplementary Material Table S13). The
BSP for the whole dataset suggests a significant population
expansion beginning much earlier than that in L. smaragda,
at around 100,000–200,000 years ago (Fig. 5). There were
clearly significant differences among the three regions of
North I., South I. and Cook Strait (Fig. 5). In the North
Island, the data suggest a recent population expansion
(around 40-fold) beginning approximately 210,000 years
ago, while in Cook Strait and South I. they suggest signifi-
cantly smaller population expansions (in the order of 10–20-
fold) that occurred significantly more recently, at around
100,000 years ago.
Discussion
This study provides insight into the genetic patterns of two
co-occurring, abundant rocky shore species that share very
similar habitats and many life-history parameters, but have
very different dispersal potentials. The results show that,
despite its roughly ten times longer pelagic larval duration
(PLD), P. elongatus, the half crab, exhibits much higher lev-
els of population structure than the cat’s eye snail, L. smar-
agda (> fivefold for mtDNA ΦST, > 50-fold for nDNA ΦST),
and support the contention that PLD can be a poor indicator
of the population structure of a species (Kelly and Palumbi
2010; Bowen et al. 2016). Instead, the results highlight that
umn indicates the different results including all populations, North
Island, Cook Strait and South Island left to right
13
105 Page 10 of 14
recent population demography may also have a strong on
contemporary population structure. The main findings are
that: (1) both species exhibit a surprising level of population
structure, (2) contrary to expectations from PLD, there was
much stronger population structure within P. elongatus, (3)
this may be due to recent demographic expansion in L. smar-
agda, and, (4) despite differences, the two species share
several major geographic discontinuities, but few genetic
boundaries are in common with those of many other co-
distributed species.
Patterns of population structure
Both species examined in this study exhibit significant lev-
els of population structure. Although we have not directly
estimated rates of gene flow here (through, for example,
extensive coalescent analyses; a difficult task to undertake
reliably here among so many sampled populations), the pat-
terns of population structure do have implications for gene
flow within each species. Notably, where there are major
genetic discontinuities between adjacent populations, this is
likely to indicate regions of lowered connectivity, at least in
the short term, as significant phylogeographic or allele fre-
quency structure cannot persist in the face of high gene flow
(Avise 2000). There is less certainty that regions of genetic
homogeneity are necessarily due to high connectivity, as
a variety of factors may drive this (including non-equilib-
rium conditions; Slatkin 1993). We were unable to sample
locations over multiple years, and thus are unable here to
determine if there are temporal changes in genetic patterns
(Pascual et al. 2016). Although the two genetic markers were
broadly in agreement in the patterns observed, there were
some differences between the loci, but these were not sys-
tematic, and appear to be largely stochastic in nature. In this
section, we summarise the geographic patterns of population
structure observed, and make comparisons between the two
study species, and with the extensive range of other species
examined in New Zealand, but note the potential implica-
tions for connectivity.
Lunella smaragda
Low levels of overall pairwise ΦST indicate that the cat’s
eye snail does not have as clear a spatial genetic structure
as other New Zealand invertebrates (Goldstien et al. 2006),
despite the short larval duration. The mtDNA pairwise dif-
ferences are similar to those in other species with much
longer PLD, such as P. regularis (ΦST = 0.072) (Waters and
Roy 2004). According to the integrated results from both
genes, the true genetic structure is complex, and the major
locations of genetic discontinuity divide the species into
four relatively distinct regions northeastern North Island
13
Marine Biology (2021) 168:105
(NE_NI), northwestern North Island (NW_NI), Cook Strait
(CS) and southern South Island (S_SI) (Fig. 3c).
At the northern tip of the North I., (location A, Fig. 3c).
it is evident that genetic differentiation is supported by both
genes, although more at the level of allele frequency dif-
ferentiation (FST) rather than phylogeographic divergence
(ΦST). This barrier was also found in other studies where
the species has low larval dispersal capabilities (Stevens and
Hogg 2004; Veale and Lavery 2012). Upwelling at the top
of Cape Reinga, combined with the predominantly southerly
flowing currents down both coasts (Stanton 1973), have been
suggested as a possible explanation for the genetic differen-
tiation observed in this area (Veale and Lavery 2011).
Results also support the hypothesis of homogeneity in
the Cook Strait region (CS), similar to that in the bivalve
P. novazelandiae (Silva and Gardner 2015). This central
group of genetically similar populations is wider in L. smar-
agda than reported in previous studies, and includes loca-
tions around Cook Strait (CS), TAR and HWB, showing
that in locations B and C (Fig. 3c) there may be barriers to
dispersal of the mollusc larvae. The western location of the
disjunction at the southern limits of the Greater Cook Strait,
location D, may correspond with that reported in many other
studies at around the 42° latitude at Cape Farewell (Apte and
Gardner 2002; Ayers and Waters 2005; Goldstien et al. 2006;
Veale and Lavery 2011). On the eastern side, there is strong
evidence from both loci that the CS region is differentiated
from the Southern South Island region (S_SI). The popula-
tions KAI and CHC were included in the larger Cook Strait
genetic region, suggesting an uncommon potential barrier
to dispersal at location E. Unlike locations A and D, this
location E is not a commonly-reported hydrographic bar-
rier, however, it was also found to be a location of genetic
discontinuity in the mollusc H. iris (Will et al. 2011). The
location of this potential barrier may be related to the major
southerly current (Southern Current) in this region, which
sweeps eastward and northward along the southeast coast
of the South I., until, at around the Christchurch Peninsula,
it moves off to the east along the Chatham Rise, perhaps
interfering with larval connectivity along this east coast. The
location also coincides with a large gap in suitable rocky
habitat.
Petrolisthes elongatus
By combining a diversity of genetic analyses from both
genes, we have developed a better understanding of the
genetic structuring of P. elongatus. P. elongatus exhibited
much greater levels of population genetic structure than
L. smaragda. At least four genetically distinctive regions
were found: North Island (NI), a central region around Cook
Strait (CS), and two South Island groups in the southwest-
ern South Island (SW_SI) and eastern South Island (E_SI)
Marine Biology (2021) 168:105
(Fig. 4c). Between the two islands, the combined genetic
results (Fig. 4c) support the existence of a relatively dis-
tinctive but homogeneous group of populations from both
northern and southern coasts of the Cook Strait area. The
southern limit of this CS group on the eastern side appears
to be located in the vicinity of Cape Campbell, and is thus
congruent with results from previous studies (Waters and
Roy 2004; Goldstien et al. 2006; Veale and Lavery 2011;
Nagel et al. 2015). Some researchers suggest the seasonal
upwelling in this area is a larval dispersal barrier. However,
upwelling cannot be presented as the direct cause of the
genetic break without a better understanding of its effects
on the dispersal capability of larvae (Ross et al. 2009). The
major currents on the eastern side, the East Cape Current
(ECC) and the Wairarapa Eddy, may also have a strong effect
on the restrictions to larval dispersal across this region (Ross
et al. 2009).
The distinct southern region, including SLO, STE and
JAC locations, showed high levels of genetic diversity within
each population and high levels of genetic differentiation
from other populations. A similar pattern has been found
in the southern populations of the New Zealand scallop
Pecten novazelandiae (Silva and Gardner 2015). This struc-
turing is possibly due to larval retention being promoted by
strong eddies in the Foveaux Strait (Chiswell and Rickard
2011; Silva and Gardner 2015). Another possible explana-
tion is the difference in times of colonisation and expansion
observed in the half-crab. According to the ‘abundant cen-
tre’ model, it is expected that peripheral populations will
exhibit higher genetic differentiation, which is exacerbated
by rapid extinction and recolonizations events (Eckert et al.
2008). This region is definitely at the extreme of the distribu-
tion of this species, which prefers warmer waters, and thus it
may be expected to show the greatest peripheral divergence
from the rest of the species due to this.
P. elongatus exhibited much greater levels of popula-
tion genetic structure than L. smaragda, despite having a
much longer PLD and breeding season. Most other relevant
aspects of their life history are similar, including habitat,
distribution, extremely large population sizes, only a larval
dispersal phase, similar breeding season and reproductive
output, and no sex bias (Grange 1976; McLay 1988). There
are some other aspects of the biology of these two species
that differ, namely external fertilisation in L. smaragda (but
occurring within 1 day of gamete release, Grange 1976),
ovigerous females and potentially greater behavioural con-
trol of dispersal in the P. elongatus pelagic larvae (McLay
1988) than the limited swimming capacity of the L. smara-
gus veliger larvae. Although the relatively short lifespans of
each animal differ to some degree (max. 2 years for P. elon-
gatus (Jones 1977) and 4–5 years for L. smaragus (Walsby
1977), both species exhibit a similar total reproductive out-
put and number of broods (between one to three times during
Page 11 of 14 105
their lifespan Jones 1977; Walsby 1977). Overall, the only
relevant differences between the species appear to be the
much longer PLD (~ tenfold) and breeding season, both of
which strongly suggest that P. elongatus has a much higher
dispersal potential.
Demographic history
Both species examined here show clear signals of high
haplotype and low nucleotide diversity, with L. smaragda
also showing a clear star-shaped haplotype network for
both mtDNA and nDNA loci, and a strong excess of low-
frequency alleles. There are several potential causes of such
patterns, the most likely being demographic history, selec-
tion, or reproductive skew (Niwa et al. 2016). Although
always a possibility, we do not expect that selection is driv-
ing these patterns. There is no other evidence that either
locus sequenced in under selection; there are no non-synon-
ymous substitutions in either species’ COI, and the strong
concordance in haplotype network between loci within
each species makes unlikely synchronous selective sweeps
in both mtDNA and nDNA. Recently, reproductive skew,
a high variance in progeny number and characteristic of
sweepstakes recruitment (Hedgecock and Pudovkin 2011),
has been implicated as a potential cause of the described pat-
terns of diversity, particularly in marine organisms with high
reproductive output (Grant et al. 2016; Niwa et al. 2016).
Although this is also a possibility in the species under study
here, analyses of the site frequency spectra (SFS, see Sup-
plementary Material Fig. S7) do not reveal the characteristic
signal of reproductive skew (a U-shaped distribution). Also,
the observed degree of excess in low-frequency mutations
would require an extreme reproductive skew (Ψ > 0.3, where
Ψ is the proportion of offspring in the population originating
from a single parent in the previous generation (Matusze-
wski et al. 2018), which is unlikely in either of these species
sampled throughout their distribution. We therefore regard
demographic history as being the most likely cause of the
observed patterns of within-population molecular diversity.
There is also a need for caution in the interpretation of
past demographic parameters from molecular data. Inferred
dates of demographic events are often likely to be over-
estimates, due to the time-dependent rate effect, where
population-level substitution rates are likely to be greater
than estimates derived from recent phylogenetic divergences
(Ho et al. 2011). The estimates used here are the least biased
possible, as they are derived from similarly recent, dated
divergences of closely-related species (Williams et al. 2011;
Hiller and Lessios 2017). Bayesian skyline plots (BSPs) also
need cautious interpretation. If sweepstakes reproduction
applies, the Fisher-Wright coalescence model used in BSPs
is likely to bias the timing of events (pushing them further
into the past), and multi-merger coalescent models may be
13
105 Page 12 of 14
more appropriate (Grant et al. 2016). Also, recent events are
likely to eliminate the signal from more distant events (Grant
2015). Despite these potential difficulties, we believe a cau-
tious, comparative interpretation of inferred demographic
parameters can provide useful additional information in such
population analyses.
If we reject selection and reproductive skew as being
likely causes, both species examined here show a clear signal
of demographic expansion over the most recent time period.
The specific substitution rate estimates allow us to estimate
the date of expansion in L. smaragda to around 40,000 years
ago, while in P. elongatus, for the overall population, this
was estimated at around 150,000 years ago. Although these
are likely to be over-estimates, they are currently the best
estimates available, do not detract from the clear relative
difference in expansion dates, and permit some comparison
with related studies. Although mismatch distribution and
BSP estimates for expansion time are slightly different, it is
clear that both methods suggest a considerably more recent
population explosion in L. smaragda. Rapid expansion and
colonisation events in recent times do not allow sufficient
time for populations to fully reach migration-drift equilib-
rium, which can result in lowered genetic diversity and weak
differentiation across the distributional range of a species
(Slatkin 1993). It is likely the recent demographic expansion
(and likely associated colonisation) within the species has
greatly influenced the homogenisation of the populations of
the mollusc, leaving little evolutionary time for genetic dif-
ferences to develop among populations. However, it appears
that even the relatively small genetic divergences that have
developed over this time largely correspond in location with
previously described marine barriers to dispersal in New
Zealand.
Interestingly, P. elongatus revealed a strong latitudinal
gradient in the time of expansion. This crustacean is perhaps
an interesting example of post-glaciation effects. The popu-
lation explosion in the Cook Strait and South Island popula-
tions occurred considerably after the demographic expansion
in North Island populations. This may reflect a greater and
more recent effect of glaciation on southern populations.
P. elongatus exhibits a clear latitudinal difference in the
period when the populations rapidly increased in size. Such
apparently climate-driven expansions have also been seen in
other species in New Zealand (Silva and Gardner 2015) and
in the northern hemisphere (Maggs et al. 2008).
Conclusions
Overall, although each species exhibited slightly different
patterns of population structure, both species exhibited
some common, previously described genetic boundaries.
This study has also highlighted that many New Zealand
13
Marine Biology (2021) 168:105
species in fact exhibit remarkably different genetic pat-
terns, which are sometimes unexpected. In the future, a
greater understanding of the major factors driving these
patterns will likely require more systematic comparisons
across a wide range of species.
The results provide strong evidence that historical pro-
cesses rather than dispersal potential are likely to most influ-
ence the difference in spatial population structure of these
two organisms. Contrary to our expectations, the levels of
population differentiation are greater in P. elongatus, with
high dispersal potential, compared to L. smaragda, with very
short-lived pelagic larvae. Both species appear to have expe-
rienced recent population expansions, but these were much
more recent in L. smaragda than in P. elongatus. We feel
that the patterns of population structure evident within each
species are likely related to regions of increased or decreased
dispersal, but that more recent demographic expansion in
L. smaragda has erased much of the expected genetic struc-
ture within that species. If our interpretations are correct, the
level of genetic population structure evident within L. smar-
agda would be expected to gradually increase in the future,
to match or surpass those of P. elongatus, as migration-drift
equilibrium is approached. This highlights the importance
of demographic history in understanding the spatial genetic
structure of species.
Supplementary Information The online version contains supplemen-
tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 00227-0​ 21-0​ 3891-2.
Acknowledgements We thank the many collaborators who assisted
with the collection of samples around the country. Special thanks to
Martin Hingston (University of Auckland) and Clinton Duffy (New
Zealand Department of Conservation) for setting the foundations of
this study. This research was supported financially by the New Zealand
Department of Conservation, the Beate Schuler Doctoral Scholarship
(to VA) and the University of Auckland. We deeply thank the reviewers
for improving the manuscript with its insightful comments.
Author contributions All authors contributed to the study conception
and design. Material preparation, data collection and analysis were per-
formed by Vibha Thakur, Shane Lavery and Vanessa Arranz. The first
draft of the manuscript was written by Vanessa Arranz and all authors
commented on previous versions of the manuscript. All authors read
and approved the final manuscript.
Funding This research was supported financially by the New Zealand
Department of Conservation, the Beate Schuler Doctoral Scholarship
in Marine Science to Vanessa Arranz and the University of Auckland.
Availability of data and material The datasets generated during the
current study are available in the GenBank repository, ACCESSION
NUMBERS for Lunella smaragda_COI: MN484628—MN485347 and
ITS: MT032725—MT033014. ACCESSION NUMBERS for Petrolis-
thes elongatus_COI: MN485348—MN485765 and ITS: MZ263776-
MZ264075. Associated metadata are also available in the Genomic
Obervatories Metadatabase (GEOME; GUID http://n​ 2t.n​ et/a​ rk:/2​ 1547/​
CmZ2 and http://​n2t.​net/​ark:/​21547/​Cmf2).
Marine Biology (2021) 168:105
Declarations
Conflict of interest The authors declare that they have no conflict of
interest.
Ethics approval No approval of research ethics committees was
required to accomplish the goals of this study because experimental
work was conducted with an unregulated invertebrate species.
Consent for publication All authors voluntary gave permission to pub-
lish all the contents of this research study.
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