The Influence of Territoriality and Mating System on the Evolution Of

doi:10.1111/j.1420-9101.2004.00823.x

The inﬂuence of territoriality and mating system on the evolution of male care: a phylogenetic study on ﬁsh

M. AH-KING, C. KVARNEMO & B. S. TULLBERG Department of Zoology, Stockholm University, Stockholm, Sweden

Keywords: Abstract certainty of paternity; Evolution of male care is still poorly understood. Using phylogenetically paternal care; matched-pairs comparisons we tested for effects of territoriality and mating sneaking; system on male care evolution in fish. All origins of male care were found in sperm competition; pair-spawning species (with or without additional males such as sneakers) and Teleostei; none were found in group-spawning species. However, excluding group territory. spawners, male care originated equally often in pair-spawning species with additional males as in strict pair-spawning species. Evolution of male care was also significantly related to territoriality. Yet, most pair-spawning taxa with male care are also territorial, making their relative influence difficult to separate. Furthermore, territoriality also occurs in group-spawning species. Hence, territoriality is not sufficient for male care to evolve. Rather, we argue that it is the combination of territoriality and pair spawning with sequential polygyny that favours the evolution of male care, and we discuss our results in relation to paternity assurance and sexual selection.

Introduction of parental care have assumed that caring for young restricts males from gaining additional matings (e.g. Parental care is common among animal taxa and has Wade & Shuster, 2002). originated numerous times. Particularly the evolution of In this study, we found at least 22 origins of male care male care has attracted much interest (e.g. Trivers, 1972; in fishes. The question arises why this is so common. Williams, 1975; Dawkins & Carlisle, 1976; Maynard First, in many fish species the assumption that giving care Smith, 1977; Ridley, 1978; Perrone & Zaret, 1979; limits the ability to attract new mates may simply not be Werren et al., 1980; Baylis, 1981; Gross & Shine, 1981; borne out. For example, for males that hold a territory in Gross & Sargent, 1985; Wright, 1998; Tallamy, 2000) and which several females may spawn in succession, the cost several factors promoting the evolution of male care have of lost mating opportunities is probably insignificant been proposed. Features that should increase the benefit (Blumer, 1979). Therefore male spawning territoriality is of caring include, for example, a harsh environment, commonly suggested to be a prerequisite for male care competition for resources, and high predation pressure evolution (Williams, 1975; Clutton-Brock, 1991). Sec- (Clutton-Brock, 1991). However, caring for young may ondly, it is often assumed that a male’s average paternity, be costly and these costs involve reduced foraging i.e. certainty of paternity of a particular offspring, will be opportunities (Trivers, 1972; Williams, 1975), increased lower than the female’s average maternity (e.g. Kokko & adult mortality (Magnhagen & Vestergaard, 1991) and, Jennions, 2003). However, in fish with male care in most importantly for males, lost mating opportunities nesting territories and several female clutches, each because of an often impaired ability to attract new mates female’s maternity may often be lower than the total (Trivers, 1972; Williams, 1975; Balshine-Earn & Earn, paternity of the caring male (C. Kvarnemo, unpub- 1998). Indeed, most models investigating the evolution lished). Territoriality has been suggested to be a precursor to male care, as the former has been assumed to ensure very high paternity (Perrone & Zaret, 1979; Baylis, 1981). Correspondence: Malin Ah-King, Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden. However, as pointed out already by Keenleyside (1981) Tel.: +46 (0) 8 16 43 98; fax: +46 (0) 8 16 77 15; this assumption is often inaccurate, as in many fishes that e-mail: [email protected] provide care in territories, paternity is often considerably

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reduced by sneakers intruding into the male-guarded territoriality and mating system for these species. How- territory. Nevertheless, territoriality is likely to increase ever, in many cases the sister group to a clade with male paternity assurance compared with nonterritoriality. care was not well studied and we had to use more distant Moreover, sexual selection can also affect male care relatives for which data were available. evolution. Females have been shown to prefer males that We defined parental care as all behaviours that might can demonstrate care-taking abilities, either through increase the fitness of the offspring, which includes for courtship behaviours (O¨ stlund & Ahnesjo¨ , 1998), nest- example nest building, bearing, guarding and fanning of building ability (Soler et al., 1998; Jones & Reynolds, eggs. However, merely building a nest could be regarded 1999) or the presence of eggs in their nests (e.g. Ridley & as mating effort rather than parental investment. There- Rechten, 1981; Marconato & Bisazza, 1986; Knapp & fore we present the results both including and excluding Sargent, 1989). Males have also been shown to use the species in which males only perform care in the form parental behaviours as a courtship strategy (e.g. of nest building. Pampoulie et al., 2004). As caring becomes attractive to We categorized the mating systems into three groups: females, this adds another benefit of care to the male, by group spawning, pair spawning, pair spawning with not only increasing offspring survival, but also increasing additional males. Group spawners spawn in a school with his mating opportunities. In fact, Tallamy (2000) has several females and males. Pair spawners include both proposed that male care could imply a benefit in terms of monogamous spawnings and sequentially polygynous increased mating success because of female preference, spawnings (i.e. matings with multiple females one at a instead of a cost (after male care has evolved). Available time). Additional males are usually sneakers or satellites. data on arthropods support the hypothesis that sexual However, this group also includes cases in which two selection has dominated the evolution of exclusive male males join a female on each side, so called trio spawnings. care (Tallamy, 2000). Data on fish in which males guard Species that are reported to be broadcasting have been their offspring also support this hypothesis, but natural categorized as group spawners. Data and references are selection has played a primary role in species that carry, presented in Appendix A1. To test the effect of mating mouth- or pouch-brood their young (M. Ah-King, system on male care we first contrasted lineages with unpublished). group spawning to all varieties of pair spawning. We then Although the evolution of male care has received compared lineages with pair spawning, by contrasting considerable interest, to our knowledge no study has yet pure pair spawning to spawning where one male and one investigated if the factors proposed to influence the origin female are accompanied by one or several additional of male care do indeed predate it. Here we test hypothe- males. ses concerning territoriality and mating system. Fish are We recorded a species as territorial if at least some an ideal group for testing these hypotheses phylogenet- males hold spawning territories, as many species have ically, because both paternal care and territoriality have both territorial and sneaker males. However, we did not evolved a number of times and a wide range of mating include pure feeding territories. We assumed that a male systems can be found in this taxon. We test the that builds a nest must be territorial during spawning hypotheses by comparing male care evolution in phylo- even if we did not find any references on territoriality in genetic lineages contrasted with respect to differences in these species. However, male parental care as such does territoriality and mating system, respectively. not necessarily imply spawning territoriality, as caring does not always involve site defence. A male can, for Material and methods instance, carry the eggs with him (seahorses and pipefish, Breder & Rosen, 1966) or splash water on the eggs above the surface (Copella arnoldi, O’Neil & Dunham, 1972). The data We used data on exclusive male care, male spawning Phylogenetic tree reconstruction territoriality and mating system, in combination with phylogenetic information, focusing in particular on We constructed a composite tree (Fig. 1) that as far as origins of exclusive male care (from no male care). We possible is based on studies that have used modern searched the literature for descriptions of paternal care, phylogenetic methods. When several phylogenies were spawning territoriality and mating system and assigned available for a group, we chose the two with the best them to categories, as described below and as summar- resolution and which included the largest number of ized in Appendix 1. Our main sources were Breder & species for which we could obtain behavioural data. Rosen (1966) and the databases Fishbase, ISI (Institute Alternative phylogenies (Fig. 2) were used to test whe- for Scientific Information) and ASFA (Aquatic Sciences ther our results were consistent between phylogenies. As and Fisheries Abstracts). To infer origins of male care, we the different alternative subtrees are independent, we collected data on species with exclusive male care and used the combination of alternative subtrees that pro- their closest relatives lacking male care, as judged by the duced the minimum and maximum number of changes phylogeny of the group. We then tried to find data on respectively in each trait.

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(a) Salmoniformes Gasterosteiformes Percidae Batrachoidae Cyprinodontiformes Coregonus lavaretus Coregonus autumnalis Coregonus artedii Thymallus thymallus Hypomesus pretiosus Mallotus villosus Esox lucius Esox niger Lota lota Lota lota maculosa Gadus morhua Porichthys notatus Percopsis omiscomaycus Menidia menidia Mugil cephalus Aulorhynchus flavidus Aulichthys japonicus Hypoptychus dybowskii Spinachia spinachia Apeltes quadracus Culaea inconstans Pungitius pungitius Gasterosteus aculeatus Syngnathus typhle Hippocampus subelongatus Solenostomus Pegasus lancifer Eurypegasus draconis Centriscidae Macroramphosus scolopax Fistularia commersonii Cyprinodon variegatus Jordanella floridae Perca fluviatilis Perca flavescens Stizostedion vitreum Stizostedion canadense Stizostedion lucioperca Etheostoma nigrum Etheostoma zonale Etheostoma spectabile Etheostoma flabellare Etheostoma caeruleum Percina maculata Percina caprodes Pleuronectes flesus

Osteoglossiformes Dipnoi Characiiformes Cyprinidae

Siluriformes Protopterus annectens Protopterus aethiopicus Lepidosiren paradoxa Neoceratodus forsteri Acipenser gueldenstaedtii Acipenser transmontanus Polyodon spathula Lepisosteus osseus Amia calva Scleropages leichardti Scleropages jardinii Scleropages formosus Osteoglossum bicirrhosum Pantodon buchholzi Chitala chitala Pollimyrus isidori Mormyrops anguilloides Silurus glanis Eigenmannia virescens Hoplias malaba Copella arnoldi Aphyocharax dentatus Brycon alburnus Pristobrycon calmoni Moxostoma carinatum Erimyzon oblongus Catostomus catostomus Cyprinus carpio Tinca tinca Brachydanio rerio Rhodeus ocellatus Pseudorasbora parva Zacco temmincki Ctenopharyngodon idella Notemigonus Scardinius erythrophthalmus Abramis brama Ptychocheilus Gila Rhinichthys Agosia Exoglossum Phenacobius Nocomis Hybognathus Campostoma Dionda Couesius Semotilus Margariscus Phoxinus phoxinus Richardsonius Clinostomus Hybopsis Ericymba Notropis Luxilus Lythrurus Cyprinella spiloptera Cyprinella lutrensis Pimephales Misgurnus anguillicaudatus Clupea harengus Coregonus - Pleuronectes

Fig. 1 Composite tree. (a) Optimization of male care. Black lines, male care; white lines, no male care; hatched lines, equivocal. (b) Optimization of male spawning territoriality. Black lines, male spawning territoriality; white lines, no male spawning territoriality; hatched lines, equivocal.

There are relatively many phylogenies that focus on (Ictaluridae). The phylogeny for Gasterosteidae was intra-familial relationships. We found a number of these obtained from McLennan et al. (1988), and alternative in Systematics, Historical Ecology, and North American Fresh- phylogenies for Characidae were found in Lucena (1993) water Fishes (Mayden, 1992): Smith (1992)(Catostomi- and Uj (1990) cited in Tree of life (Ortı´ & Vari, 1997). For dae), Cavender & Coburn (1992) and Coburn & the relationships among darters (Percidae) we used Cavender (1992) (Cyprinidae), and Lundberg (1992) Turner (1997) and Song et al. (1998). The relationships

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(b) Salmoniformes Gasterosteiformes Percidae Batrachoidae Cyprinodontiformes Coregonus lavaretus Coregonus autumnalis Coregonus artedii Thymallus thymallus Hypomesus pretiosus Mallotus villosus Esox lucius Esox niger Lota lota Lota lota maculosa Gadus morhua Porichthys notatus Percopsis omiscomaycus Menidia menidia Mugil cephalus Aulorhynchus flavidus Aulichthys japonicus Hypoptychus dybowskii Spinachia spinachia Apeltes quadracus Culaea inconstans Pungitius pungitius Gasterosteus aculeatus Syngnathus typhle Hippocampus subelongatus Solenostomus Pegasus lancifer Eurypegasus draconis Centriscidae Macroramphosus scolopax Fistularia commersonii Cyprinodon variegatus Jordanella floridae Perca fluviatilis Perca flavescens Stizostedion vitreum Stizostedion canadense Stizostedion lucioperca Etheostoma nigrum Etheostoma zonale Etheostoma spectabile Etheostoma flabellare Etheostoma caeruleum Percina maculata Percina caprodes Pleuronectes flesus

Osteoglossiformes Dipnoi Characiiformes Cyprinidae

Fig. 1 Continued. between families and orders are less well resolved. We Patterson, 1996). For the relationships within Osteoglos- used Fink & Fink (1981) for the relationships within siformes we used Lauder & Liem (1983), Nelson (1994), Ostariophysi. Clupeomorpha was positioned as a sister Kumazawa & Nishida (2000) and Lavoue´ et al. (2000). group of Ostariophysi according to Lecointre & Nelson Alternative phylogenies of Gasterosteiformes were found (1996). Salmonids were placed together with osmerids as in Pietsch (1978), Johnson & Patterson (1993) and a sister group of esocoids and neoteleosts (Johnson & Nelson (1994). In addition, Smith & Stearley (1989)

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Osteoglossiformes Dipnoi Characiiformes Cyprinidae

Siluriformes Protopterus annectens Protopterus aethiopicus Lepidosiren paradoxa Neoceratodus forsteri Acipenser gueldenstaedtii Acipenser transmontanus Polyodon spathula Lepisosteus osseus Amia calva Scleropages leichardti Scleropages jardinii Scleropages formosus Osteoglossum bicirrhosum Pantodon buchholzi Chitala chitala Pollimyrus isidori Mormyrops anguilloides Silurus glanis Eigenmannia virescens Hoplias malaba Copella arnoldi Aphyocharax dentatus Brycon alburnus Pristobrycon calmoni Moxostoma carinatum Erimyzon oblongus Catostomus catostomus Brachydanio rerio Cyprinus carpio Tinca tinca Rhodeus ocellatus Pseudorasbora parva Zacco temmincki Ctenopharyngodon idella Scardinius erythrophthalmus Abramis brama Ptychocheilus Gila Rhinichthys Agosia Exoglossum Phenacobius Nocomis Hybognathus Campostoma Dionda Couesius Semotilus Margariscus Phoxinus phoxinus Richardsonius Clinostomus Hybopsis Ericymba Notropis Luxilus Lythrurus Cyprinella spiloptera Cyprinella lutrensis Pimephales Misgurnus anguillicaudatus Clupea harengus Coregonus - Pleuronectes

Fig. 2 Alternative composite tree. (a) Opti- mization of male care. Black lines, male care; white lines, no male care; hatched lines, equivocal. (b) Optimization of male spawning territoriality. Black lines, male spawning territoriality; white lines, no male spawning territoriality; hatched lines, equivocal. was used for the relationships within Salmoniformes, formes, Amia, Lepisosteidae and Teleostei were posi- Parker & Kornﬁeld (1995) for the relationships within tioned according to Nelson (1994) and Bemis et al. Cyprinodontiformes and Grande & Bemis (1996) for the (1997), and ﬁnally Johnson & Patterson (1993) proposed relationships within Acipenseriformes. Cobitidae was a scheme for the relationships within Percomorpha, included in Cypriniformes (Nelson, 1994). Acipenseri- which we have used.

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Osteoglossiformes Dipnoi Characiiformes Cyprinidae Siluriformes Protopterus annectens Protopterus aethiopicus Lepidosiren paradoxa Neoceratodus forsteri Acipenser gueldenstaedtii Acipenser transmontanus Polyodon spathula Lepisosteus osseus Amia calva Scleropages leichardti Scleropages jardinii Scleropages formosus Osteoglossum bicirrhosum Pantodon buchholzi Chitala chitala Pollimyrus isidori Mormyrops anguilloides Silurus glanis Eigenmannia virescens Hoplias malaba Copella arnoldi Aphyocharax dentatus Brycon alburnus Pristobrycon calmoni Moxostoma carinatum Erimyzon oblongus Catostomus catostomus Brachydanio rerio Cyprinus carpio Tinca tinca Rhodeus ocellatus Pseudorasbora parva Zacco temmincki Ctenopharyngodon idella Scardinius erythrophthalmus Abramis brama Ptychocheilus Gila Rhinichthys Agosia Exoglossum Phenacobius Nocomis Hybognathus Campostoma Dionda Couesius Semotilus Margariscus Phoxinus phoxinus Richardsonius Clinostomus Hybopsis Ericymba Notropis Luxilus Lythrurus Cyprinella spiloptera Cyprinella lutrensis Pimephales Misgurnus anguillicaudatus Clupea harengus Coregonus - Pleuronectes

Fig. 2 Continued.

additional males. We dealt with equivocal branches by Optimization of characters using two extreme solutions, either maximizing or The characters were optimized using parsimony in minimizing male care branches over the whole tree. MacClade 4.0 (Maddison & Maddison, 2000). We opti- The same method was used for equivocal optimizations mized mating system as a two state-character, group of mating system and territoriality. The number of origins spawning and pair spawning with or without sneakers/ shown in the results are the minimum and maximum

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numbers, which depend on which particular optimiza- Table 1 Matched-pairs with respect to the presence/absence of tion and phylogeny that was used. When a character territoriality. The presence of male care origins is compared within optimization for a polytomy (i.e. when the phylogenetic each pair. Ranges in male care origins and alternative matched pairs relationships are not resolved for three or more species) are due to alternative phylogenies and/or to equivocal parts of the tree resulting in alternative optimizations. Male care originates more was equivocal, we used the most parsimonious optimi- often in the territorial group in each of the 15 comparisons involving zation. For example, in a polytomy of three species for a difference in male care origins (sign test: C 14 ¼ 0, P < 0.001). which no care was inferred to be the ancestral state, and Post-ovipositional male care (excluding cases with nest-building where male care was present in two and absent in one only, indicated by *) originates more often in the territorial group in species, we assumed that male care had evolved only each of the 12 pairs with a difference in origins of post-ovipositional once. male care (sign test: C 11 ¼ 0, P < 0.01).

Paired taxa No. of origins of male care Matched pairs comparisons 1. Territorial: Protopterus–Neoceratodus 1 As explained above, we collected data on male care, Nonterritorial: Acipenser–Polyodon 0 territoriality and mating system and constructed two 2. Territorial: Amia calva 1 alternative composite trees, based on the species with Nonterritorial: Lepisosteus osseus 0 such information. Territoriality and mating system were 3. Territorial: Scleropages–Mormyrops 2–3 optimized using maximum parsimony and these varia- Nonterritorial: Clupea 0 4. Territorial: Silurus–Eigenmannia 1 bles were considered independent in separate analyses. Nonterritorial: Aphylocharax–Pristobrycon 0 The optimizations were used to identify independent 5. Territorial*: Hoplias 0 matched pairs contrasted by alternate states, following Nonterritorial*: Copella 0 the logic first presented by Burt (1989) (see also Møller & 6. Territorial: Moxostoma, Erimyzon 1 Birkhead, 1992; Wickman, 1992; Reed & Nee, 1995; Nonterritorial: Catostomus 0 Lindenfors & Tullberg, 1998; Goodwin et al., 2002). For 7 or 8 and 9: each comparison, the paths linking the taxa do not cross 7. Territorial: Rhodeus, Pseudorasbora 1 the path of another comparison, and thus the compar- Nonterritorial: Ptycocheilus 0 isons are phylogenetically separate (Felsenstein, 1985; 8. Territorial: Rhodeus 0 Burt, 1989; Reed & Nee, 1995; Purvis & Bromham, 1997; Nonterritorial: Tinca 0 9. Territorial: Pseudorasbora 1 Maddison, 2000). Once a matched pair has been iden- Nonterritorial: Ptychocheilus 0 tified it cannot be accounted for again and comparisons 10. Territorial: Zacco 0 are sought among taxa that are as closely related as Nonterritorial: Ctenopharyngodon 0 possible in the remaining phylogeny (see for example 11. Territorial: Abramis 0 Lindenfors et al., 2003). Therefore a matched pair need Nonterritorial*: Notemigonus or Scardinius 0 not be sister clades. Thereafter, instances of transitions to 12. Territorial: Rhinichthys, Agosia 1 male parental care were scored within each contrast, Nonterritorial: Gila 0 under the null hypothesis that transitions from nonpa- 13. Territorial: Exoglossum–Margariscus 2–3 rental (the presumed ancestral state) to male care would Nonterritorial: Phoxinus 0 be independent of the state for either territoriality or 14. Territorial: Campostoma, Dionda 1 Nonterritorial: Hybognathus 0 mating system. A simple binomial test was used to test 15. Territorial: Notropis 0 the null hypothesis. One important confounding factor in Nonterritorial: Ericymba 0 this analysis is the size of the contrasting clades, such that 16. Territorial: Luxilus–Pimephales 1+1 more speciose clades would have a higher background Nonterritorial: Richardsonius, Clinostomus 0 probability of transitions to male care. To partially 17. Territorial: Thymallus 0 compensate for the lack of data on species number we Nonterritorial: Coregonus 0 have compared whether or not male care has evolved in 18. Territorial: Porichthys 1 each contrasting clade instead of the number of times this Nonterritorial: Percopsis or Lota, Gadus 0 has occurred, using a sign test. 19. Territorial: Aulorhynchus–Gasterosteus 1–2 Nonterritorial: Syngnathus–Fistularia 1 20. Territorial: Cyprinodon, Jordanella 1 Results Nonterritorial: Menidia–Mugil 0 21. Territorial: Stizostedion lucioperca 1 Male care has evolved in a few nonterritorial taxa such as Nonterritorial: S. vitreum or S. canadense 0 Copella arnoldi and Syngnathidae. However in the major- 22. Territorial: Etheostoma nigrum–E. zonale 1 ity of cases territoriality has preceded male care (Figs 1 Nonterritorial: E. spectabile 0 and 2) and in an analysis based on phylogenetically 23. Territorial: Etheostoma flabellare 1 independent comparisons male care is significantly more Nonterritorial: E. caeruleum 0 likely to evolve in territorial than nonterritorial lineages *Male care originates in the ancestor to Hoplias and Copella. (C 14 ¼ 0, P < 0.001; Table 1). Because nest building can Origin of male nest building (no post-ovipositional care).

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be regarded as merely mating effort we also carried out Table 2 Male care origins in matched-pair comparisons of mating an analysis based on male post-oviposition care only and systems. Group spawning (G) is contrasted against pair spawning found that male care thus defined was also significantly with or without sneakers/additional males (P). The presence of male more likely to evolve in territorial lineages (C 11 ¼ 0, care origins are compared within each pair. Ranges in male care origins and alternative matched pairs are due to alternative phylo- P < 0.01; Table 1). genies and/or to equivocal parts of the tree resulting in alternative In our data set we found no case where male parental optimizations. Male care originates in the pair spawning group with care has evolved in a group spawning species, and when or without sneakers/additional males in each of the 16–17 compar- contrasting group spawning with different kinds of pair isons where there is a difference in male care origins (sign test: C 15– spawning in a matched-pairs comparison, we found that 16 ¼ 0, P < 0.001). Post-ovipositional male care (excluding taxa in male care evolution is significantly related to pair which male care consists of only nest-building, indicated by asterisks) spawning (C 15–16 ¼ 0, P < 0.001; Table 2). This was originates in the pair spawning species with or without sneakers/ also the case when only taxa with post-oviposition male additional males in each of the 12–13 comparisons where there is a care were included (C 11–12 ¼ 0, P < 0.01; Table 2). difference in male care origins (sign test: C 11–12 ¼ 0, P < 0.01). More interesting, perhaps, is the question of whether No. of origins the occurrence of male parental care in pair-spawning Paired taxa of male care species is influenced by the occurrence of additional males such as sneakers. Therefore, we also conducted a 1 or 2 and 3: test where we excluded all group-spawning taxa and 1. P: Protopterus–Neoceratodus 1 G: Acipenser–Polyodon 0 contrasted pair spawning with and without sneakers in 2. P: Amia calva 1 phylogenetically matched pairs. In our data set there G: Lepisosteus osseus 0 were only six such contrasts, and in two of these male 3. P: Scleropages–Mormyrops 2–3 care originated in the lineage without sneakers whereas G: Acipenser–Polyodon 0 in four it evolved in the lineage with sneakers (C 5 ¼ 2, 4. P: Silurus glanis, Eigenmannia 1 n.s.; Table 3). Only considering post-ovipositional care G: Clupea 0 (i.e. excluding nest building only) produced the same 5. P: Hoplias–Copella 1 result (C 7 ¼ 3, n.s.; Table 3). Thus, judged from this G: Aphyocharax–Pristobrycon 0 limited set of observations we conclude that the evolu- 6. P: Erimyzon, Moxostoma, Catostomus 1* tion of male care is independent of whether a male can G: Brachydanio–Cyprinus 0 7 or 8 and 9: monopolize a female during spawning or not. 7. P: Rhodeus ocellatus, Pseudorasbora parva 1 G: Notemigonus–Clinostomus 0 Discussion 8. P: Rhodeus ocellatus 0 G: Tinca tinca 0 In this study, we found a strong effect of both mating 9. P: Pseudorasbora parva 1 system and territoriality on the evolution of paternal care G: Scardinius–Clinostomus 0 in fishes. Basically, paternal care does not evolve under 10. P: Zacco temminicki 0 group spawning, but only in species with pair spawning, G: Ctenopharyngodon idella 0 even when this involves additional males such as 11. P: Agosia 1* sneakers. That male care evolves more often in territorial G: Rhinichthys 0 12. P: Exoglossum 1 species has often been assumed, but to our knowledge G: Phenacobius 0 not previously been tested. Furthermore, Ridley (1978) 13. P: Campostoma 1* pointed out that territoriality could have evolved sec- G: Dionda 0 ondarily after male care, as well as before, so that 14. P: Nocomis 1 territoriality could be a result of male care rather than a G: Hybognathus 0 cause of it. However, our results show that the majority 15. P: Semotilus 1 of male care origins were preceded by spawning territo- G: Couesius 0 riality. In the following we discuss our results in relation 16. P: Luxilus 1* to parental certainty and sexual selection. G: Lythrurus or Hybopsis–Notropis 0 The low degree of paternal certainty in group spawn- 17 or 18 and 19: 17. P: Cyprinella spiloptera, 1 ings is probably the reason why paternal care does not C. lutrensis, Pimephales promelas evolve under this mating system, and because parental G: Lythurus 0 certainty is low for both sexes the same result is expected 18. P: Cyprinella spiloptera 0 for all kinds of parental care. However, our results show G: C. lutrensis 0 clearly that parental certainty need not be complete, such 19. P: Pimephales promelas 1 as when a female is monopolized, but that male care can G: Lythurus 0 evolve also under pair spawning where there are addi- 20. P: Thymallus thymallus 0 tional males present. In species with male care and G: Coregonus lavaretus, C. autumnalis, C artedii 0 sneakers, however, the paired male has been found to

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Table 2 Continued. fertilize a majority of the eggs under natural spawning conditions: 81% in bluegill sunfish (Fu et al., 2001) and No. of origins 89% in sand gobies (Jones , 2001). Nevertheless, Paired taxa of male care et al. sneakers might compensate their lower fertilization 21. P: Mallotus 0 probability in a particular spawning by participating in G: Hypomesus 0 a larger number of spawnings. In bluegill sunfish, for 22. P: Pleuronectes 0 example, sneakers and guarding males have similar G: Esox 0 individual fitnesses (Neff, 2001). In the few contrasts 23. P: Porichthys notatus 1 with pair spawning that differed with respect to addi- G: Percopsis omiscomaycus or Gadus morhua 0 24. P: Lota lota lota 0 tional males (Table 3), the difference in male care origins G: Lota lota maculosa 0 was not significant. In other words, at this point we 25. P: Aulorhynchus–Jordanella 3–4 cannot say that paternity is important, within the range G: Menidia menidia, Mugil cephalus 0 of variation that occurs in pair spawning, for the 26. P: Sander lucioperca 1 evolution of male care. However, this question needs G: Stizostedion vitreum or S. canadense 0 further investigation using an extended data set. 27. P: Etheostoma nigrum, E. zonale, 2 The male-caring species in our analysis are both pair E. spectabile, E. flabellare spawning and (with a few exceptions such as pipefishes G: E. caeruleum 0 and seahorses, Appendix 1, Table 2) territorial. Thus, it 28. P: Percina maculata, Percina caprodes 0 could be argued that it is pair spawning as such that is G: Perca 0 important for the evolution of paternal care and not *Origin of male nest building (no post-ovipositional care). territoriality. Indeed, because many group spawners are territorial as well, and paternal care never evolves in group spawners, we hold that territoriality is not a sufficient condition for male care to evolve. Instead, we Table 3 Male care origins in matched-pair comparisons of pair reckon that it is the combination of territoriality with pair spawning groups with or without sneakers/additional males. Pair spawning that has favoured the evolution of paternal spawning (P) is contrasted against pair spawning with sneakers (S) care. Then, why are these conditions important for male or trio spawning (T). Ranges are due to alternative phylogenies or care? optimizations. In two of the comparisons male care origin is more We believe that paternity is likely to increase above a common without sneakers and in four comparisons it is more certain minimum threshold under a combination of pair- common in the presence of sneakers (sign test: C 5 ¼ 2, n.s.). The spawning and territoriality. This is so because under corresponding numbers for origins of post-oviposition care (excluding taxa in which male care consists of only nest-building, indicated these circumstances a male may both be better able to by asterisks) are three and five comparisons, respectively (sign test: guard his mate against other males, and to spawn C 7 ¼ 3, n.s.). sequentially with multiple females, in which case the cost of male care in terms of missed opportunities to mate Paired taxa No. of origins of male care becomes very low (Loiselle, 1978; Gross & Sargent, 1. P: Misgurnus 0 1985). In our sample of care-giving species such males T/S: Moxostoma–Zacco 1+1* were reported to mate with several, in some cases up to 2. P: Exoglossum, Nocomis 1–2 seven, females as in Spinachia spinachia (Jones et al., S: Campostoma 1* 1998), and in Hypoptychus dybowskii males have been 3. P: Luxilus 1* reported to guard 30 egg masses (Narimatsu & Mune- S: Semotilus 1 hara, 2001). Thus, care giving under pair spawning and 4. P: Cyprinella spiloptera 0 territoriality is fully compatible with a high degree of S: Pimephales 1 polygyny. 5. P: Lota lota lota 0 Some of our analyses included only post-mating care, S: Porichthys 1 6. P : Culaea 0 i.e. we excluded species that only built nests. For these S : Pungitius 0 species, too, territoriality was a strong predictor of male 7. P: Syngnathus–Eurypegasus 1 care. In a recent model Wade & Shuster (2002) S: Macroramphosus 0 concluded that if only some males are successful in 8. P: Pleuronectes 0 mating, these males will have higher average reproduc- S: Aulorhynchus–Gasterosteus 1–2 tive rate than females and will thereby gain more by 9. P: Jordanella 1 deserting the young. Wade & Shuster (2002) also argued S: Cyprinodon 0 that their analysis supports the hypothesis that there is a 10. P: Percina maculata 0 trade-off between pre-mating investment in competition S: P. caprodes 0 and post-mating investment in offspring care (Wade, *Origin of male nest building (no post-ovipositional care). 1979). Most ESS models of the evolution of uniparental Male care is already present in the ancestor to this group. care assume that caring is incompatible with continued

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mating (Maynard Smith, 1977; Wade & Shuster, 2002). Jacob Ho¨ glund, Arne Mooers, John Reynolds, Tom As this is not the case in fishes, our results are not in Tregenza and Lars Werdelin provided very helpful accordance with Wade’s hypothesis, because then we comments on earlier versions of the manuscript. This would predict that territorial males are less likely to work was financially supported by the Swedish Research invest in the care of young. Instead, as mentioned, Council (grants to CK and to BT) and the Foundation of territoriality probably lowers the cost of care (Loiselle, Emil and Lydia Kinander, and was in part done while CK 1978; Gross & Sargent, 1985) and the ability to guard was on a post-doc at the University of Jyva¨skyla¨, Finland. multiple clutches eliminates the conflict between mating effort and parental effort. Supplementary material In addition, if caring becomes attractive to females, male care could imply a benefit in terms of increased The following material is available from http:// mating success because of female preference, instead of a www.blackwellpublishing.com/products/journals/suppmat/ cost (Tallamy, 2000). Possibly, certain aspects of male jeb/jeb823/jeb823sm.htm care can also improve paternity. For example, a nest Appendix A1 Mating systems, parental care, male structure may help the male to defend his brood, not territoriality and references used. only against predators, but also against sneaker males. Consistent with this, sand goby males have been shown to build extra small nest openings before mating when References sneaker males are present (Svensson & Kvarnemo, Balshine-Earn, S. & Earn, D.J.D. 1998. On the evolutionary 2003). Once parental care has evolved, there is probably pathway of parental care in mouth-brooding cichlid fish. Proc. a feedback between the levels of care and the intensity of R. Soc. Lond. B. 265: 2217–2222. sexual selection (Reynolds, 1996). For example, the Baylis, J.R. 1981. The evolution of parental care in fishes, with variance in male reproductive success (and thus the reference to Darwin’s rule of male sexual selection. Env. Biol. intensity of sexual selection) could increase when males Fish. 6: 223–251. care, especially if females prefer to mate with males that Bemis, W.E., Findeis, E.K. & Grande, L. 1997. An overview of already guard eggs from other females in their nests (e.g. Acipenseriformes. Env. Biol. Fish. 48: 25–71. Ridley & Rechten, 1981; Marconato & Bisazza, 1986; Blumer, L.S. 1979. Male parental care in the bony fishes. Q. Rev. Knapp & Sargent, 1989). Indeed, a comparative study on Biol. 54: 149–161. Breder, C.M. & Rosen, D.E. 1966. Modes of Reproduction in Fishes. fish suggests that female choice of caring males has been The Natural History Press, Garden City. important for the evolution of male care among Burt, A. 1989. Comparative methods using phylogenetically egg-guarding species (M. Ah-King unpublished). Species independent contrasts. In: Oxford Surveys in Evolutionary that care for eggs by carrying them on the body or in Biology, Vol. 6 (P. H. Harvey & L. Partridge, eds), pp. 33–53. mouth- or brood pouches, on the other hand, have Oxford University Press, Oxford. limited space for the eggs, which suggests that sexual Cavender, T.M. & Coburn, M.M. 1992. Phylogenetic relation- selection may have been less important for the evolution ships of North American Cyprinidae. In: Systematics, Historical of male care in these species. Ecology and North American Freshwater Fishes (R. L. Mayden, Male care has evolved many times in fish and we ed.), pp. 293–327. 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