
==== Front
Sci Rep
Sci Rep
Scientific Reports
2045-2322
Nature Publishing Group UK London

39251772
71541
10.1038/s41598-024-71541-w
Article
The deeper the rounder: body shape variation in lice parasitizing diving hosts
Leonardi María Soledad 1
Paz Rodrigo R. 23
Oliveira Hugo Luiz 4
Lazzari Claudio R. 5
Negrete Javier 67
Márquez Federico fede@cenpat-conicet.gob.ar

18
1 https://ror.org/03cqe8w59 grid.423606.5 0000 0001 1945 2152 Instituto de Biología de Organismos Marinos (IBIOMAR), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Boulevard Brown 2915, PC 9120 Puerto Madryn, Chubut Argentina
2 grid.455453.6 0000 0004 0485 1240 ANSYS Inc., 7374 Las Positas Rd., Livermore, California 94551 USA
3 https://ror.org/03cqe8w59 grid.423606.5 0000 0001 1945 2152 IMIT, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Av. Libertad 5460, 1er. piso, W3404AAS Corrientes, Corrientes Argentina
4 grid.411087.b 0000 0001 0723 2494 FECFAU, Departamento de Estruturas, Universidade Estadual de Campinas (UNICAMP), Avenida Albert Einstein, 951, Campinas, São Paulo 13083-852 Brazil
5 grid.12366.30 0000 0001 2182 6141 Institut de Recherche sur la Biologie de l’Insecte-UMR CNRS 7261, University of Tours, 37200 Tours, France
6 https://ror.org/01tjs6929 grid.9499.d 0000 0001 2097 3940 Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, 122 and 60, PC 1900 La Plata, Buenos Aires Argentina
7 https://ror.org/02vyk6z19 grid.469960.4 0000 0004 0445 9505 Departamento de Biología de Predadores Tope, Instituto Antártico Argentino, Cerrito 1248, PC 1010 Buenos Aires, Argentina
8 https://ror.org/022g6pv04 grid.440495.8 0000 0001 2220 0490 Universidad Nacional de la Patagonia San Juan Bosco, Boulevard Brown 3051, PC 9120 Puerto Madryn, Chubut Argentina
9 9 2024
9 9 2024
2024
14 2094721 5 2024
28 8 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Seal lice, unique among insects, show remarkable adaptability to the extreme conditions of the deep sea. Evolving with their seal and sea lion hosts, they have managed to tolerate hypoxia, high salinity, low temperature, and elevated hydrostatic pressure. Given the diving capabilities of their mammalian hosts, which can reach depths of hundreds to thousands of meters, our study examines the morphological variation among closely related seal lice species infesting hosts with different maximum diving depths. In particular, our research reveals a significant morphological difference between lice associated with regular and deep-diving hosts, where lice from deep-diving hosts tend to be rounder. This could be an adaptation to withstand the high hydrostatic pressures found in the deep ocean. The rounded shape optimizes the louse’s ability to withstand external pressure by redistributing it over a larger ventral/dorsal plane. This in turn minimizes the internal energy required to support body deformations, thereby increasing the louse’s resilience in the deep sea environment.

Keywords

Diving adaptations
Marine insects
Morphometrics
Seal lice
Pinnipeds
Subject terms

Biophysics
Ecology
Evolution
Zoology
http://dx.doi.org/10.13039/501100003074 Agencia Nacional de Promoción Científica y Tecnológica PICT 2015- 0082 PICT 2018-0537 PICT 2020-0400 Leonardi María Soledad PADI FoundationLerner-Greyissue-copyright-statement© Springer Nature Limited 2024
==== Body
pmcIntroduction

The colonization of the oceans by marine mammals has had a significant impact on the parasitic fauna associated with them. Several authors1–4 have hypothesized that the ocean acted as an ecological barrier for parasites during the transition from land. However, in the case of pinnipeds, they have preserved some taxa of originally terrestrial parasites. Remarkably, sucking lice are among those parasites that have successfully co-evolved and diversified in close association with their mammalian hosts.

Sucking lice are obligate haematophagous insects that live as permanent ectoparasites in the fur or hair of their mammalian hosts, attached to the skin. The family Echinophthiriidae (Phthiraptera: Anoplura) comprises a remarkable group of species that infest amphibious hosts, such as pinnipeds (walruses, seals and sea lions) and river otters5,6. Pinnipeds are diving mammals, and some of them, such as sea lions and fur seals typically dive to ∼100 m, while true seals can reach depths exceeding 1000 m7,8. The most exceptional diving seal is the southern elephant seal Mirounga leonina, which may dive beyond 2000 m depth8.

During the evolutionary transition of pinnipeds from land to sea, echinophthiriid lice have had to cope with the gradual transition to an amphibian lifestyle together with their hosts, some of which manage to spend more than 80% of their time submerged and perform frequent extreme dives7,8. These obligate and permanent ectoparasites have adapted to tolerate hypoxia, high salinity, low temperature and even very high hydrostatic pressure9. Many questions remain as to how do lice manage survive the challenges of the marine environment, and what morphological, physiological and behavioral adaptations are responsible for their success as the only insects capable of surviving in the depths of the ocean.

Concerning lice’s morphological adaptations, only the presence of scales over the body has been the object of attention, resulting in different hypotheses advanced by Murray10 and by Hinton11 relative to their function. According to the literature, the main features of seal lice are (1) a large development of legs, strongly adapted to grasp hair fibers; (2) spiracles with an elaborate closing device that could preserve atmospheric air in the tracheal system and prevent the entry of seawater during immersion; (3) a membranous and thick abdomen, the significance of which is not clear9. However, it is clear that seal lice have faced strong developmental constraints and selective pressures during their evolution.

The adaptation of the body form to specific bio-mechanical constraints can be analyzed by evaluating using an approach of geometric morphometrics, since allometric growth in different species can be associated with shifts in environmental conditions across their evolutive history, favoring traits that optimize individual survival (see Gould12 among others). In this study, we investigated the morphological variability of closely related seal lice species infesting hosts with different diving habits, in order to quantify the phenotype-environment co-variation of these unique marine insects. On the other hand, we propose a physical hypothesis regarding the hydrodynamic and hydrostatic lice body shape adaptation.

Material and methods

Sampling

A total of 130 adult lice were collected from five host seals species (Table 1). Table 1 Lice species and their host analyzed in this study.

Louse species	Code	n	Host	Max/average diving depth (m)	Average host body mass (kg)	
Male	Female	
Lepidophthirus macrorhini	Lm	45	Elephant seals	2388/549.8±84.1 8,13	2998	688	
Antarctophthirus carlinii	Ac	26	Weddell seal	700/458±113 14	425	450	
Antarctophthirus ogmorhini	Ao	2	Leopard seal	424/44±48 15	300	325	
Antarctophthirus lobodontis	Al	29	Crabeater seal	776/248±141 16	232	249	
Antarctophthirus microchir	Am	28	South American sea lion	256/158±32 17	325	145	

Capturing the body shape and size

Lice 2D images were photographed using a Carl Zeiss binocular magnifying glass equipped with AxioVision Rel.4.5 software (©Carl Zeiss Imaging Solutions) in order to obtain the body ventral view (Fig. 1).Fig. 1 Ventral aspect and wire-frame of the louse Antarctophthirus lobodontis showing the position of the 27 landmarks and 16 semi-landmarks used to perform geometric morphometric analysis. These landmarks are: (1) the anterior edge of the head, (2–4) semi-landmarks placed between landmark 1 and 5, (5) end of postantennal angle, (6) posterior base of the first segment of the antenna, (7) anterior extreme of the first coxal condyle, (8) base of the first coxal condyle, (9) posterior extreme of the first coxal condyle, (10) anterior extreme of the second coxal condyle, (11) base of the second coxal condyle, (12) posterior extreme of the second coxal condyle, (13) anterior extreme of the third coxal condyle, (14) base of the third coxal condyle, (15) posterior extreme of the third coxal condyle, (16–26) semi-landmarks around the abdomen outline, (21) apex of the abdomen, (27) posterior extreme of the left third coxal condyle, (28) base of the left third coxal condyle, (29) anterior extreme of the left third coxal condyle, (30) posterior extreme of the left second coxal condyle, (31) base of the left second coxal condyle, (32) anterior extreme of the left second coxal condyle, (33) posterior extreme of the left first coxal condyle, (34) base of the left first coxal condyle, (35) anterior extreme of the left first coxal condyle, (36) posterior base of the left first segment of the antenna, (37) end of left post antennal angle, (38–40) semi-landmarks placed between landmark 1 and 37, (41) maximum curvature of the neck, (42) anterior base of the first segment of the antenna, and (43) anterior base of the left first segment of the antenna. Scale bar = 1 mm.

Lice were placed with their dorsal side facing down to avoid pitching or rolling effects. We capture the lice ventral body shape using the following landmark and semi-landmark configuration illustrated in Fig. 1. One observer (FM) made the digitization process using TPSDig2 software18. Due to the lice body shape presents object symmetry19, a perpendicular axis of bilateral symmetry (left-right axis) that was defined between landmarks 1, 41, and 21. To standardize, translation, rotation, and scale in a symmetry object, we made a Procrustes fit with reflection20. Then, the variation around the mean shape was decomposed into the symmetric and asymmetric components20,21. Due to our interest is in symmetry, the asymmetric variation components were dismissed. Previously, to homologate semi-landmarks, we used a mathematical algorithm that slid each semi-landmark in an iterative process, minimizing the TPS function’s bending energy. To do this we used TpsRelw software22. The centroid size, the square root of the sum of the squared distances from the landmarks to the centroid which they define, was used as a proxy for size23.

Statistical analyses

The statistical analyses for geometric morphometrics analyses were performed in the MorphoJ, version 1.07a24. To evaluate and control the allometry effect (change in the lice shape related to size increment), a pooled-seal lice species multivariate regression between aligned Procrustes coordinates (dependent variables) and centroid sizes (independent variable) was calculated, running a permutation test (10,000 rounds).

The principal component analysis of the variance-covariance matrix was done to explore and display the major features of the seal lice body shape23. Then, to display axes of maximum discrimination among seal lice species shapes, we performed a canonical variate analysis (CVA). Finally, to test statistical differences among seal lice species, we used a cluster analysis UPGMA-MDGC25,26. This method successfully determines the number of groups based on inferential statistics in hierarchical cluster analysis. The graphical output of the MDGC test is a useful tool since it shows a clear distinction between statistically different groups as well as their relationships27.

Results

Seal louse body size (centroid size) differed significantly among species (H=60.49, p<0.0001). Lice from elephant seals were bigger than the others (Fig. 2).Fig. 2 Body size (CS) variations between seals lice species. The central dot represents the mean; the median is represents as a central line; the limits of the box, the first and third quartiles, and the whiskers the 95% confidence interval; the dots out the whiskers are outliers. Different letters indicate significant differences (p < 0.05) in pairwise comparisons test. Am: Antarctophthirus microchir, Al: Antarctophthirus lobodontis, Lm: Lepidophthirus macrorhini, Ac: Antarctophthirus carlinii, and Ao: Antarctophthirus ogmorhini.

Seal lice growth was allometric. The relationship between body shape and size pooled within seal lice species was statistically significant (permutation test with 10,000 random permutations, p<0.0001) and accounted for 11.72% of the shape variation (Fig. S.1, Supplementary Material section A). Therefore, the regression residuals were used as free-allometric shape variables in subsequent statistical analyses.

Principal component (PC) analysis of body shape variation showed that 82.62% of the total shape variation was concentrated in the first three PC scores. Interpretation of shape variation using wire-frame plots showed that PC1 (which explained 50.25% of the total variance) was related to body slenderness, which was associated with posterior expansion and rostral development. Individuals at the positive extreme were associated with a rounded body shape, exhibited lateral rostral and lateral expansion, posterior constriction, and posteriorly directed expansion of the coxae. In contrast, individuals at the negative extreme showed speculative variations in body shape (slender). Individuals at the positive extreme of PC2 (25.25%) showed right-left lateral constrictions and less rostral development. On the contrary, individuals from the negative extreme showed the opposite shape variations (Fig. 3).Fig. 3 Plot of the first two principal components (PC1 versus PC2) for different species of lice, based on Procrustes distances. The figures represent the displacement vectors from the overall mean shape (gray wire-frame) to the positive and negative extreme shape (black wire-frame) for each PC. Shape changes have been exaggerated (scale factor: SF±0.1) in the graphic for better visualization. Percentages of explained variance for each axis are in parentheses.

CVA showed that lice body shape can be successfully used to discriminate between species. Pairwise comparisons of Mahalanobis distances between the five lice species revealed significant differences in mean body shape (Table 1). Values of CV1 (89.77%) separated Lepidophthirus macrorhini (positive values) from the others, with a more rounded posterior part, a posterior projection of the coxae and an expanded rostrum. While CV2 (8.41%) separated Antarctophthirus microchir (negative values) from the other lice species of the genus Antarctophthirus (positive values), L. macrorhini was found in between, close to the consensus shape. CV2 variation was associated with robust (positive values) to slender body shapes (Fig. 4). Hierarchical clustering using the cutting criteria from the MDGC test indicated three groups (p<0.05), one of host Antarctic seal lice, one of South American sea lions and one of elephant seals (Fig. 5). The Antarctic seal host group showed no significant differences in lice body shape (p>0.05). This large group was linked to the group formed by the three species of the Antarctophthirus genera. The most divergent group is Lepidophthirus macrorhini, the louse that parasitises the deeper-diving species.Fig. 4 Canonical variate analysis showing the maximum separation of ventral shape differences among lice species. Wire-frame show shape changes from mean shape (gray vectors) to the positive and negative extreme (black vectors) in both axis.

Fig. 5 Cluster diagram showing the ventral shape relationships among lice species and the overlapped wire-frames of the reconstructed consensus configurations to each ones. The cut-off criterion (p=0.05) obtained with the MDGC test is indicated with a horizontal line. Three statistically different groups of ventral shapes were identified by this method.

Discussion

This study used geometric morphometrics to compare the variation in the shape of different species of seal lice. We also provide compelling graphical and analytical evidence that these species differ in allometric growth forms. We hypothesize that shape reflects environmental constraints and adaptation to marine conditions. Indeed, our results showed a tendency for those species with deeper diving behavior to be more rounded.

A general rule for parasites, known as Harrison’s rule, states that large-bodied host species have large-bodied parasite species28,29. This relationship has been demonstrated in a wide variety of parasitic taxa, including worms, crustaceans, fleas, flies, lice, ticks, aphids, beetles, flies, thrips, flower mites and moths30–36. Harrison described this pattern by analyzing avian lice, and it is in this group that it is most well documented37. In fact, the rule has been demonstrated in 581 species of bird lice belonging to dozens of genera38. For sucking lice, Cannon39 found that they conform to Harrison’s rule, at least in the three families analyzed. Our results are partially consistent with this general rule. We found that lice from elephant seals were bigger but also rounder than the others.

On the other hand, parasites allocate much more resources to attachment structures or organs40. For example, in intestinal parasites, attachment organs increase disproportionately with body size because the greater the size, the greater the risk of detachment40. In feather lice, the ability to attach is not a determinant of host specificity, even though lice have a long co-evolutionary history with their hosts41,42. The same appears to be true for seal lice. Our results do not show a higher development of legs or claws. In Lepidophthirus macrorhini we found a posteriorly directed extension of the coxae. In contrast to most echinophthiriids, the first pair of legs in this species are robust and the tarsal claw is modified into a well-developed nail. This difference in the function of the first pair may explain the position and development of the coxae.

Although four of the five species analyzed belong to the same genus, it is important to note the differences between the hosts. Three groups can be distinguished. Antarctophthirus microchir, which infects sea lions; the Antarctic seal lice, including A. lobodontis, A. weddelli, and A. ogmorhini; and L. macrorhini from the southern elephant seal. These groups were successfully distinguished by the body shape of the lice. Lepidophthirus macrorhini has a more rounded posterior part, a posterior projection of the coxae and an expanded rostrum. While A. microchir could be separated from the other Antarctophthiruses by CV2. CV2 variation was associated with robust to slender body shapes. Different allometric relationships may reflect selective pressures and elucidate past evolutionary trends, especially in related species40. In particular, parasites may allocate more resources to the growth of structures whose importance scales allometrically with size40. As we mentioned above, an example of this is the size of attachment organs. In general, parasites display a wide range of body shapes and sizes as well as differences in anatomical structures40. However, how these shapes are modeled by selective pressure remains unclear.

Although other organisms living permanently in high hydrostatic pressure environments in the deep sea and abyssopelagic zone have not all evolved round shapes, sea lice have been subject to different selective pressures that have affected their body allometry compared to them. In particular, the forces acting on their bodies change rapidly over a wide range. Close to the surface they experience atmospheric pressure, but at maximum diving depths they can be exposed to hydrostatic pressures of 200–250 atm.

From a physical point of view, the rounded shape of an insect can help it to adapt better to high hydrostatic pressures due to structural advantages. An increased area on its ventral/dorsal plane (Fig. S.2 Supplementary Material section B) allows the external pressure to be better redistributed along the entire body volume, reducing the internal energy expended to support the body deformations undergone, making a louse with a larger wet area better able to withstand the external pressure. As an increase in external pressure is proportional to surface area (and not volume), an oblate individual will experience less energy expenditure due to pressure compression than an elongated (prolate) shape. This characteristic of deep-diving lice may be related to hydrostatic pressure at great depths.

Supplementary Information

Supplementary Information 1.

Supplementary Information 2.

Supplementary Information

The online version contains supplementary material available at 10.1038/s41598-024-71541-w.

Acknowledgements

The study was financially and logistically supported by the Dirección Nacional del Antártico, Instituto Antártico Argentino. The permit for this work was granted by the Dirección Nacional del Antártico (Environmental Office).

Author contributions

MSL: Conceptualization, Data Curation, Methodology, Investigation, Validation, Visualization, Writing – Original Draft, Writing – Review & Editing. RRP: Conceptualization, Data Curation, Formal Analysis, Physics Solver, Validation, Visualization, Writing Original Draft, Writing – Review & Editing. HLO: Formal Analysis, Physics Solver, Validation, Visualization, Writing Original Draft, Writing – Review & Editing. CL: Conceptualization, Investigation, Writing – Original Draft, Writing – Review & Editing. JN: Data Curation, Investigation, Writing Original Draft, Writing – Review & Editing. FM: Conceptualization, Data Curation, Formal Analysis, Methodology, Software, Validation, Visualization, Writing – Original Draft, Writing – Review & Editing. All authors contributed critically to the drafts and gave final approval for publication.

Funding

This research was funded by the Agencia de Promoción Científica Tecnológica (PICT 2015-0082, PICT 2018-0537, PICT 2020-0400), PADI Foundation and the Lerner-Grey Fund for Marine Research.

Data availability

The data described in this article can be freely and openly accessed as Supplementary material.

Competing interests

The authors declare no competing interests.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
==== Refs
References

1. Holberg E Recognition of larvae of the tetrabothriidae (eucestoda): Implications for the origin of tapeworms in marine homeotherms Can. J. Zool. 1987 65 997 1000 10.1139/z87-158
Holberg, E. Recognition of larvae of the tetrabothriidae (eucestoda): Implications for the origin of tapeworms in marine homeotherms. Can. J. Zool. 65, 997–1000 (1987).10.1139/z87-158
2. Balbuena J Raga J Intestinal helminth communities of the longfinned pilot whale (globicephala melas) off the faroe islands Parasitology 1993 106 327 333 10.1017/s0031182000075156 8488068
Balbuena, J. & Raga, J. Intestinal helminth communities of the longfinned pilot whale (globicephala melas) off the faroe islands. Parasitology 106, 327–333. 10.1017/s0031182000075156 (1993).8488068 10.1017/s0031182000075156
3. Aznar F Balbuena J Raga J Helminth communities of Pontoporia blainvillei (cetacea: Delphinidae) in Argentinian and Uruguayan waters Can. J. Zool. 1994 72 443 448 10.1139/z94-094
Aznar, F., Balbuena, J. & Raga, J. Helminth communities of Pontoporia blainvillei (cetacea: Delphinidae) in Argentinian and Uruguayan waters. Can. J. Zool. 72, 443–448. 10.1139/z94-094 (1994).10.1139/z94-094
4. Aznar, F., Balbuena, J., Fernandez, M. & Raga, J. Living together: The parasites of marine mammals. Mar. Mammals Biol. Conserv. 385–423 (2002).
5. Durden L Musser G The sucking lice (insecta, anoplura) of the world: A taxonomic checklist with records of mammalian hosts and geographical distributions Bull. Am. Mus. Nat. 1994 218 1 90
Durden, L. & Musser, G. The sucking lice (insecta, anoplura) of the world: A taxonomic checklist with records of mammalian hosts and geographical distributions. Bull. Am. Mus. Nat. 218, 1–90 (1994).
6. Leonardi M Palma R Review of the systematics, biology and ecology of lice from pinnipeds and river otters (insecta: Phthiraptera: Anoplura: Echinophthiriidae) Zootaxa 2013 3630 445 466 10.11646/zootaxa.3630.3.3 26131525
Leonardi, M. & Palma, R. Review of the systematics, biology and ecology of lice from pinnipeds and river otters (insecta: Phthiraptera: Anoplura: Echinophthiriidae). Zootaxa 3630, 445–466. 10.11646/zootaxa.3630.3.3 (2013).26131525 10.11646/zootaxa.3630.3.3
7. Stewart B Encyclopedia of Marine Mammals, Chap. Diving Behavior 2009 Academic Press 321 327
Stewart, B. Encyclopedia of Marine Mammals, Chap. Diving Behavior 321–327 (Academic Press, 2009).
8. McIntyre T A lifetime at depth: Vertical distribution of southern elephant seals in the water column Polar Biol. 2010 33 1037 1048 10.1007/s00300-010-0782-3
McIntyre, T. et al. A lifetime at depth: Vertical distribution of southern elephant seals in the water column. Polar Biol. 33, 1037–1048. 10.1007/s00300-010-0782-3 (2010).10.1007/s00300-010-0782-3
9. Leonardi M Crespo J Soto F Lazzari C How did seal lice turn into the only marine insects? Insects. 2022 10.3390/insects13010046 35447793
Leonardi, M., Crespo, J., Soto, F. & Lazzari, C. How did seal lice turn into the only marine insects?. Insects.[SPACE]10.3390/insects13010046 (2022).35447793 10.3390/insects13010046
10. Murray M Marine Insects, Chap. Insect Parasite of Marine Bird and Mammals 1976 American Elsevier Publishing Company Inc 78 96
Murray, M. Marine Insects, Chap. Insect Parasite of Marine Bird and Mammals 78–96 (American Elsevier Publishing Company Inc, 1976).
11. Hinton H Marine Insects, Chap. Respiratory Adaptations of Marine insects 1976 American Elsevier Publishing Company Inc 43 78
Hinton, H. Marine Insects, Chap. Respiratory Adaptations of Marine insects 43–78 (American Elsevier Publishing Company Inc, 1976).
12. Gould S Ontogeny Phylogeny 1977 Harvard University Press
Gould, S. Ontogeny Phylogeny (Harvard University Press, 1977).
13. Costa D Huckstadt L Crocker D McDonald M Goebel BI Fedak M Approaches to studying climatic change and its role on the habitat selection of Antarctic pinnipeds Integr. Comp. Biol. 2010 50 1018 1030 10.1093/icb/icq054 21558256
Costa, D. et al. Approaches to studying climatic change and its role on the habitat selection of Antarctic pinnipeds. Integr. Comp. Biol. 50, 1018–1030. 10.1093/icb/icq054 (2010).21558256 10.1093/icb/icq054
14. Nachtsheim D Foraging behaviour of Weddell seals (Leptonychotes weddellii) in connection to oceanographic conditions in the southern weddell sea Progress Oceanogr. 2019 173 165 179 10.1016/j.pocean.2019.02.013
Nachtsheim, D. et al. Foraging behaviour of Weddell seals (Leptonychotes weddellii) in connection to oceanographic conditions in the southern weddell sea. Progress Oceanogr. 173, 165–179. 10.1016/j.pocean.2019.02.013 (2019).10.1016/j.pocean.2019.02.013
15. Kuhn C Diving physiology and winter foraging behavior of a juvenile leopard seal (Hydrurga leptonyx) Polar Biol. 2006 29 303 307 10.1007/s00300-005-0053-x
Kuhn, C. et al. Diving physiology and winter foraging behavior of a juvenile leopard seal (Hydrurga leptonyx). Polar Biol. 29, 303–307. 10.1007/s00300-005-0053-x (2006).10.1007/s00300-005-0053-x
16. Nachtsheim D Jerosch K Hagen W Plötz J Bornemann H Habitat modelling of crabeater seals (Lobodon carcinophaga) in the weddell sea using the multivariate approach maxent Polar Biol. 2017 40 961 976 10.1007/s00300-016-2020-0
Nachtsheim, D., Jerosch, K., Hagen, W., Plötz, J. & Bornemann, H. Habitat modelling of crabeater seals (Lobodon carcinophaga) in the weddell sea using the multivariate approach maxent. Polar Biol. 40, 961–976. 10.1007/s00300-016-2020-0 (2017).10.1007/s00300-016-2020-0
17. Baylis A Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion Oecologia 2015 179 1053 1065 10.1007/s00442-015-3421-4 26323982
Baylis, A. et al. Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion. Oecologia 179, 1053–1065. 10.1007/s00442-015-3421-4 (2015).26323982 10.1007/s00442-015-3421-4
18. Rohlf, F. TPSDig2 (Version 2.30) (2017).
19. Savriama Y Klingenberg C Beyond bilateral symmetry: Geometric morphometric methods for any type of symmetry BMC Evol. Biol. 2011 11 280 10.1186/1471-2148-11-280 21958045
Savriama, Y. & Klingenberg, C. Beyond bilateral symmetry: Geometric morphometric methods for any type of symmetry. BMC Evol. Biol. 11, 280. 10.1186/1471-2148-11-280 (2011).21958045 10.1186/1471-2148-11-280
20. Klingenberg C Barluenga M Meyer A Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry Evolution 2002 56 1909 1920 10.1111/j.0014-3820.2002.tb00117.x 12449478
Klingenberg, C., Barluenga, M. & Meyer, A. Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry. Evolution 56, 1909–1920. 10.1111/j.0014-3820.2002.tb00117.x (2002).12449478 10.1111/j.0014-3820.2002.tb00117.x
21. Klingenberg C McIntyre G Geometric morphometrics of developmental instability: Analyzing patterns of fluctuating asymmetry with procrustes methods Evolution 1998 52 1363 1375 10.1111/j.1558-5646.1998.tb02018.x 28565401
Klingenberg, C. & McIntyre, G. Geometric morphometrics of developmental instability: Analyzing patterns of fluctuating asymmetry with procrustes methods. Evolution 52, 1363–1375. 10.1111/j.1558-5646.1998.tb02018.x (1998).28565401 10.1111/j.1558-5646.1998.tb02018.x
22. Rohlf, F. TPSDig2 (Version 1.67) (2017).
23. Zelditch M Swiderski D Sheets H Fink W Geometric Morphometrics for Biologists: A Primer 2012 Elsevier Academic Press
Zelditch, M., Swiderski, D., Sheets, H. & Fink, W. Geometric Morphometrics for Biologists: A Primer (Elsevier Academic Press, 2012).
24. Klingenberg C Morphoj: An integrated software package for geometric morphometrics Mol. Ecol. Resources 2011 11 353 357 10.1111/j.1755-0998.2010.02924.x
Klingenberg, C. Morphoj: An integrated software package for geometric morphometrics. Mol. Ecol. Resources 11, 353–357. 10.1111/j.1755-0998.2010.02924.x (2011).10.1111/j.1755-0998.2010.02924.x
25. Valdano S Di Rienzo J Discovering meaningful groups in hierarchical cluster analysis. an extension to the multivariate case of a multiple comparison method based on cluster analysis InterStat 2007 4 1 28
Valdano, S. & Di Rienzo, J. Discovering meaningful groups in hierarchical cluster analysis. an extension to the multivariate case of a multiple comparison method based on cluster analysis. InterStat. 4, 1–28 (2007).
26. Márquez F Van Der Molen S Intraspecific shell-shape variation in the razor clam Ensis macha along the Patagonian coast J. Molluscan Studies 2011 77 123 128 10.1093/mollus/eyq044
Márquez, F. & Van Der Molen, S. Intraspecific shell-shape variation in the razor clam Ensis macha along the Patagonian coast. J. Molluscan Studies 77, 123–128. 10.1093/mollus/eyq044 (2011).10.1093/mollus/eyq044
27. Márquez F González-José R Bigatti G Combined methods to detect pollution effects on shell shape and structure in neogastropods Ecol. Indicators 2011 11 248 254 10.1016/j.ecolind.2010.05.001
Márquez, F., González-José, R. & Bigatti, G. Combined methods to detect pollution effects on shell shape and structure in neogastropods. Ecol. Indicators 11, 248–254. 10.1016/j.ecolind.2010.05.001 (2011).10.1016/j.ecolind.2010.05.001
28. Harrison L Mallophaga from apteryx, and their significance; with a note on the genus rallicola Parasitology 1915 8 88 100 10.1017/S0031182000010428
Harrison, L. Mallophaga from apteryx, and their significance; with a note on the genus rallicola. Parasitology 8, 88–100. 10.1017/S0031182000010428 (1915).10.1017/S0031182000010428
29. Bush S Clayton D The role of body size in host specificity: Reciprocal transfer experiments with feather lice Evolution 2006 60 2158 2167 17133872
Bush, S. & Clayton, D. The role of body size in host specificity: Reciprocal transfer experiments with feather lice. Evolution 60, 2158–2167 (2006).17133872
30. Harvey PH Keymer AE Comparing life histories using phylogenies Philos. Trans. R. Soc. Lond. Series B 1991 332 31 39 10.1098/rstb.1991.0030
Harvey, P. H. & Keymer, A. E. Comparing life histories using phylogenies. Philos. Trans. R. Soc. Lond. Series B 332, 31–39 (1991).10.1098/rstb.1991.0030
31. Kirk W The size relationship between insects and their hosts Ecol. Entomol. 1991 16 351 359 10.1111/j.1365-2311.1991.tb00227.x
Kirk, W. The size relationship between insects and their hosts. Ecol. Entomol. 16, 351–359. 10.1111/j.1365-2311.1991.tb00227.x (1991).10.1111/j.1365-2311.1991.tb00227.x
32. Thompson J The Coevolutionary Process 1994 Univ. of Chicago Press
Thompson, J. The Coevolutionary Process (Univ. of Chicago Press, 1994).
33. Sasal P Trouvé S Müller-Graf C Morand S Specificity and host predictability: A comparative analysis among monogenean parasites of fish J. Animal Ecol. 1999 68 437 444 10.1046/j.1365-2656.1999.00313.x
Sasal, P., Trouvé, S., Müller-Graf, C. & Morand, S. Specificity and host predictability: A comparative analysis among monogenean parasites of fish. J. Animal Ecol. 68, 437–444. 10.1046/j.1365-2656.1999.00313.x (1999).10.1046/j.1365-2656.1999.00313.x
34. Morand S Hafner M Page R Reed D Comparative body size relationships in pocket gophers and their chewing lice Biol. J. Linnean Soc. 2000 70 239 249 10.1111/j.1095-8312.2000.tb00209.x
Morand, S., Hafner, M., Page, R. & Reed, D. Comparative body size relationships in pocket gophers and their chewing lice. Biol. J. Linnean Soc. 70, 239–249. 10.1111/j.1095-8312.2000.tb00209.x (2000).10.1111/j.1095-8312.2000.tb00209.x
35. Johnson K Bush S Clayton D Correlated evolution of host and parasite body size: Tests of harrison’s rule using birds and lice Evolution 2005 59 1744 1753 10.1111/j.0014-3820.2005.tb01823.x 16329244
Johnson, K., Bush, S. & Clayton, D. Correlated evolution of host and parasite body size: Tests of harrison’s rule using birds and lice. Evolution 59, 1744–1753. 10.1111/j.0014-3820.2005.tb01823.x (2005).16329244 10.1111/j.0014-3820.2005.tb01823.x
36. Poulin R Evolutionary Ecology of Parasites 2017 Princeton University Press
Poulin, R. Evolutionary Ecology of Parasites (Princeton University Press, 2017).
37. Clayton, D., Bush, S. & Johnson, K. Coevolution of life on hosts: Integrating ecology and history. in Interspecific Interactions (University of Chicago Press, 2015).
38. Harnos A Size matters for lice on birds: Coevolutionary allometry of host and parasite body size Evolution 2017 71 421 431 10.1111/evo.13147 27925167
Harnos, A. et al. Size matters for lice on birds: Coevolutionary allometry of host and parasite body size. Evolution 71, 421–431. 10.1111/evo.13147 (2017).27925167 10.1111/evo.13147
39. Cannon, S. Size correlations between sucking lice and their hosts including a test of Harrison’s rule. Master’s thesis, Georgia Southern University, Statesboro, GA (2010).
40. Poulin R Interspecific allometry of morphological traits among trematode parasites: Selection and constraints Biol. J. Linnean Soc. 2009 96 533 540 10.1111/j.1095-8312.2008.01163.x
Poulin, R. Interspecific allometry of morphological traits among trematode parasites: Selection and constraints. Biol. J. Linnean Soc. 96, 533–540. 10.1111/j.1095-8312.2008.01163.x (2009).10.1111/j.1095-8312.2008.01163.x
41. Clayton D Bush S Johnson K Ecology of congruence: Past meets present Syst. Biol. 2004 53 165 173 10.1080/10635150490265102 14965911
Clayton, D., Bush, S. & Johnson, K. Ecology of congruence: Past meets present. Syst. Biol. 53, 165–173. 10.1080/10635150490265102 (2004).14965911 10.1080/10635150490265102
42. Bush S Sohn E Clayton D Ecomorphology of parasite attachment: Experiments with feather lice J. Parasitol. 2006 92 25 31 10.1645/GE-612R.1 16629310
Bush, S., Sohn, E. & Clayton, D. Ecomorphology of parasite attachment: Experiments with feather lice. J. Parasitol. 92, 25–31 (2006).16629310 10.1645/GE-612R.1
